Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organization

Abstract

Arabidopsis and Medicago truncatula represent sister clades within the dicot subclass Rosidae. We used genetic map-based and bacterial artificial chromosome sequence-based approaches to estimate the level of synteny between the genomes of these model plant species. Mapping of 82 tentative orthologous gene pairs reveals a lack of extended macrosynteny between the two genomes, although marker collinearity is frequently observed over small genetic intervals. Divergence estimates based on non-synonymous nucleotide substitutions suggest that a majority of the genes under analysis have experienced duplication in Arabidopsis subsequent to divergence of the two genomes, potentially confounding synteny analysis. Moreover, in cases of localized synteny, genetically linked loci in M. truncatula often share multiple points of synteny with Arabidopsis; this latter observation is consistent with the large number of segmental duplications that compose the Arabidopsis genome. More detailed analysis, based on complete sequencing and annotation of three M. truncatula bacterial artificial chromosome contigs suggests that the two genomes are related by networks of microsynteny that are often highly degenerate. In some cases, the erosion of microsynteny could be ascribed to the selective gene loss from duplicated loci, whereas in other cases, it is due to the absence of close homologs of M. truncatula genes in Arabidopsis.

Figure 1

Chromosomal alignments between the M. truncatula genetic linkage groups 1 to 4 and the Arabidopsis chromosomes. Homologs between the two genomes are connected with lines. The markers with green color are putative orthologous loci. Red lines indicate the possible syntenic relationships between the two genomes.

Figure 2

Microsynteny between sequenced M. truncatula BACs and segments of Arabidopsis chromosomes. The orientations of predicted genes are indicated by arrows. Letters A through I in A represent the nine unique gene homologies found between Arabidopsis and M. truncatula and thus define the minimum structure of the ancestral chromosome segment from which all the syntenic blocks were derived. A detailed description of gene annotations and homologies is given in Table II. The maps are drawn to scale.

Figure 3

Reconstruction of the predicted ancestral AHC locus representing five segments from the M. truncatula and Arabidopsis genomes. The transcriptional orientations of the genes are indicated by arrows. Letters A through I are consistent with those in Figure 2.

Figure 4

Phylogeny versus gene structure of syntenic and non-syntenic homologous genes. Phylogenetic analyses of protein sequences were performed using the ClustalX program (Thompson et al., 1997), and trees were constructed using the neighbor-joining method. The intron-exon structures of genes are drawn to scale. Exons are shown as boxes and introns are shown as lines. Intron-exon structures were inferred based on comparison of EST and genomic sequence data and based on gene prediction tools, as described in “Materials and Methods.” The predicted structure of Mt-TC22007 is from TIGR database, and the intron sizes are unknown.