Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis

Abstract

Synteny between soybean and Arabidopsis was studied by using conceptual translations of DNA sequences from loci that map to soybean linkage groups A2, J, and L. Synteny was found between these linkage groups and all four of the Arabidopsis chromosomes, where GenBank contained enough sequence for synteny to be identified confidently. Soybean linkage group A2 (soyA2) and Arabidopsis chromosome I showed significant synteny over almost their entire lengths, with only 2-3 chromosomal rearrangements required to bring the maps into substantial agreement. Smaller blocks of synteny were identified between soyA2 and Arabidopsis chromosomes IV and V (near the RPP5 and RPP8 genes) and between soyA2 and Arabidopsis chromosomes I and V (near the PhyA and PhyC genes). These subchromosomal syntenic regions were themselves homeologous, suggesting that Arabidopsis has undergone a number of segmental duplications or possibly a complete genome duplication during its evolution. Homologies between the homeologous soybean linkage groups J and L and Arabidopsis chromosomes II and IV also revealed evidence of segmental duplication in Arabidopsis. Further support for this hypothesis was provided by the observation of very close linkage in Arabidopsis of homologs of soybean Vsp27 and Bng181 (three locations) and purple acid phosphatase-like sequences and homologs of soybean A256 (five locations). Simulations show that the synteny and duplications we report are unlikely to have arisen by chance during our analysis of the homology reports.

Figure 1

Synteny between soyA2 and arabI. BACs showing homology to soybean sequences are indicated with lines connecting them to their soybean homolog(s). The soyA2 map at the right shows the modern linkage group, with each locus that was analyzed in this study indicated. The proposed progenitor soyA2 in the middle shows a rearranged soyA2 that maximizes the synteny with arabI. Soybean Vsp27 and AP cannot be distinguished at this level of analysis; this ambiguity is indicated by broken lines connecting Arabidopsis BAC F2 M11 and the two soybean loci. The Arabidopsis map is drawn inverted relative to the usual presentation. Tic marks and numbers indicate 10-cM intervals on arabI. The previously identified regions of homeology between soybean linkage groups (3) are identified and shown as vertical lines to the right of soyA2.

Figure 2

SoyA2 is shown with the proposed progenitor locus order (see Fig. 1). Only those loci that had significant homology to Arabidopsis sequences on arabIV or arabV are connected by lines, although tic marks for every soybean sequence analyzed are shown on the proposed progenitor soyA2 map. Thin lines indicate soybean sequences that had homologs on only one Arabidopsis chromosome. Broken lines are used to indicate uncertainty in syntenic relationships because of duplicated loci in soybean. Known genes in Arabidopsis are shown in bold type. Tic marks and numbers indicate 10-cM intervals on the Arabidopsis chromosomes. (A) Synteny between loci on soybean linkage group A2 and duplicated segments of Arabidopsis chromosomes IV and V. (B) Synteny between soybean linkage group A2 and duplicated segments of Arabidopsis chromosomes I and V.

Figure 3

Proposed evolutionary derivation of related regions of Arabidopsis chromosomes I, IV, and V. Green and orange are used to help track chromosomal segments only and do not necessarily indicate related functionality. In this model, an ancestral chromosome or chromosomal segment (protochromosome) was duplicated, producing lineages that culminated in parts of the modern Arabidopsis chromosomes I, IV, and V. In the arabIV/V lineage the path leading to arabIV branched off before the final inversion occurred. Vsp is used in the figure for both AP similarity and sequence homology to the soybean Vsp27 gene. Tic marks and numbers on the modern Arabidopsis chromosomes indicate 10-cM intervals.

Figure 4

Synteny between parts of homeologous soybean linkage groups J and L and duplicated segments of Arabidopsis chromosomes II and IV located at approximately 80 and 10 cM, respectively. Homologous sequences are connected by solid lines. Homologs in Arabidopsis to soybean sequences Sct_046 and A060 are located on a single BACs on both arabII and arabIV.

Figure 5

Locations of AP- and PAP-like sequences and homologs to soybean Vsp27, A256, and Bng181 on Arabidopsis chromosomes. Numbers on the maps show an approximate scale in centimorgans. Arabidopsis homologs to soybean AP/Vsp27 and A256 are tightly linked in three locations. Arabidopsis homologs to PAP and soybean Bng181 are tightly linked at five locations.