The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications

Abstract

Background: Rice is an important staple food and, with the smallest cereal genome, serves as a reference species for studies on the evolution of cereals and other grasses. Therefore, decoding its entire genome will be a prerequisite for applied and basic research on this species and all other cereals.

Results: We have determined and analyzed the complete sequences of two of its chromosomes, 11 and 12, which total 55.9 Mb (14.3% of the entire genome length), based on a set of overlapping clones. A total of 5,993 non-transposable element related genes are present on these chromosomes. Among them are 289 disease resistance-like and 28 defense-response genes, a higher proportion of these categories than on any other rice chromosome. A three-Mb segment on both chromosomes resulted from a duplication 7.7 million years ago (mya), the most recent large-scale duplication in the rice genome. Paralogous gene copies within this segmental duplication can be aligned with genomic assemblies from sorghum and maize. Although these gene copies are preserved on both chromosomes, their expression patterns have diverged. When the gene order of rice chromosomes 11 and 12 was compared to wheat gene loci, significant synteny between these orthologous regions was detected, illustrating the presence of conserved genes alternating with recently evolved genes.

Conclusion: Because the resistance and defense response genes, enriched on these chromosomes relative to the whole genome, also occur in clusters, they provide a preferred target for breeding durable disease resistance in rice and the isolation of their allelic variants. The recent duplication of a large chromosomal segment coupled with the high density of disease resistance gene clusters makes this the most recently evolved part of the rice genome. Based on syntenic alignments of these chromosomes, rice chromosome 11 and 12 do not appear to have resulted from a single whole-genome duplication event as previously suggested.

Figure 1

Display of features on rice chromosomes 11 and 12. Using a false-color display, we plotted features present on rice chromosomes 11 and 12. Select genetic markers are plotted with their cM positions noted; physical gaps are plotted with the centromere gap noted in red; gene density (GD) is plotted in two tracks (all genes and non-TE-related genes); expression density is determined by aligment to ESTs; transposable element (TE) density is plotted with a separate track for MITEs; tRNAs are the transfer RNAs, and the CP and MT represent chloroplast and mitochondrial insertions.

Figure 2

Presence of potential homologs in rice chromosomes 11 and 12 with other model organisms. BLASTP was used to search the proteomes of the listed model organisms and with the non-TE-related proteins from chromosomes 11 and 12. The number of proteins with matches at the designated E-value cutoffs are plotted for each model organism.

Figure 3

Frequency distribution of different categories of R-like genes and defense response genes on rice chromosomes 11 and 12. The miscellaneous category includes genes showing high homology with putative disease resistance proteins and defense response category includes genes showing high homology to chitinases, glucanases and thaumatin-like proteins. (LZ, leucine zipper; NBS, nucleotide binding site; LRR, leucine rich repeat; TM, trans-membrane).

Figure 4

Distribution pattern of resistance genes and defense response genes on rice chromosomes 11 (A) and 12 (B). Each gene category is color coded and plotted on the rice chromosome bar with respect to its cM position. Width of the vertical colored bars is proportional to the number of genes located at that position.

Figure 5

Plot of a portion of the rice chromosome 11 showing tandem arrays of disease resistance and defense response genes between positions 112.0 – 119.0 cM. The category of genes is color-coded and the arrowheads depict their direction. The numbers indicate cumulative number of all the genes predicted by TIGR on chromosome 11. The scale is based on number of genes such that the space occupied by one arrowhead corresponds to one gene, genes in the gap between arrowheads do not match with R-like genes and large gaps of unmatched genes are marked by a double slash (//).

Figure 6

Array sizes of tandemly repeated genes on rice chromosomes 11 and 12. Total tandemly amplified genes on 11 are 924 or 29% of the total genes; total tandemly amplified genes on 12 are 684 or 24% of the total genes.

Figure 7

Chromosome 12 sequences were used as query against a database of chromosome 11 sequences using MegaBLAST as described under Methods. At ≥50% coverage and >80% identity, the frequency distribution of unique duplicate gene models is plotted over the length of chromosomes 11 and 12. Based on the chromosomal locations of these unique genes, duplications were identified throughout the length of both the chromosomes. The maximum extent of duplication, however, was found to be confined within the first 2 Mb region of both chromosomes.

Figure 8

Gene duplication between rice chromosomes 11 and 12 over the whole length (a) and in the first 3 Mb region (b). Blue and red lines connect duplicate gene models in the same and opposite orientation, respectively.

Figure 9

Syntenic mapping of rice genes from rice chromosomes 11 and 12 to wheat. Distribution of the rice gene homologues from rice chromosomes 11 (blue bars) and 12 (yellow bars) on to the wheat chromosomes of seven homoeologous groups.