Organization and molecular evolution of a disease-resistance gene cluster in coffee trees

BACKGROUND: Most disease-resistance (R) genes in plants encode NBS-LRR proteins and belong to one of the largest and most variable gene families among plant genomes. However, the specific evolutionary routes of NBS-LRR encoding genes remain elusive. Recently in coffee tree (Coffea arabica), a region spanning the S(H)3 locus that confers resistance to coffee leaf rust, one of the most serious coffee diseases, was identified and characterized. Using comparative sequence analysis, the purpose of the present study was to gain insight into the genomic organization and evolution of the S(H)3 locus. RESULTS: Sequence analysis of the S(H)3 region in three coffee genomes, E(a )and C(a )subgenomes from the allotetraploid C. arabica and C(c )genome from the diploid C. canephora, revealed the presence of 5, 3 and 4 R genes in E(a), C(a), and C(c )genomes, respectively. All these R-gene sequences appeared to be members of a CC-NBS-LRR (CNL) gene family that was only found at the S(H)3 locus in C. arabica. Furthermore, while homologs were found in several dicot species, comparative genomic analysis failed to find any CNL R-gene in the orthologous regions of other eudicot species. The orthology relationship among the S(H)3-CNL copies in the three analyzed genomes was determined and the duplication/deletion events that shaped the S(H)3 locus were traced back. Gene conversion events were detected between paralogs in all three genomes and also between the two sub-genomes of C. arabica. Significant positive selection was detected in the solvent-exposed residues of the S(H)3-CNL copies. CONCLUSION: The ancestral S(H)3-CNL copy was inserted in the S(H)3 locus after the divergence between Solanales and Rubiales lineages. Moreover, the origin of most of the S(H)3-CNL copies predates the divergence between Coffea species. The S(H)3-CNL family appeared to evolve following the birth-and-death model, since duplications and deletions were inferred in the evolution of the S(H)3 locus. Gene conversion between paralog members, inter-subgenome sequence exchanges and positive selection appear to be the major forces acting on the evolution of S(H)3-CNL in coffee trees.