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

Ribas AF, Cenci A, Combes MC, Etienne H, Lashermes P - BMC Genomics (2011)

Bottom Line: All these R-gene sequences appeared to be members of a CC-NBS-LRR (CNL) gene family that was only found at the SH3 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.Gene conversion between paralog members, inter-subgenome sequence exchanges and positive selection appear to be the major forces acting on the evolution of SH3-CNL in coffee trees.

View Article: PubMed Central - HTML - PubMed

Affiliation: IRD - Institut de Recherche pour le Développement, UMR RPB, Montpellier Cedex, France.

ABSTRACT

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 SH3 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 SH3 locus.

Results: Sequence analysis of the SH3 region in three coffee genomes, Ea and Ca subgenomes from the allotetraploid C. arabica and Cc genome from the diploid C. canephora, revealed the presence of 5, 3 and 4 R genes in Ea, Ca, and Cc 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 SH3 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 SH3-CNL copies in the three analyzed genomes was determined and the duplication/deletion events that shaped the SH3 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 SH3-CNL copies.

Conclusion: The ancestral SH3-CNL copy was inserted in the SH3 locus after the divergence between Solanales and Rubiales lineages. Moreover, the origin of most of the SH3-CNL copies predates the divergence between Coffea species. The SH3-CNL family appeared to evolve following the birth-and-death model, since duplications and deletions were inferred in the evolution of the SH3 locus. Gene conversion between paralog members, inter-subgenome sequence exchanges and positive selection appear to be the major forces acting on the evolution of SH3-CNL in coffee trees.

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BAC clone contigs spanning the SH3 locus. BAC clones spanning the SH3 locus as previously contigued [46]. Sequenced BACs from the three genomes are indicated by gray boxes.
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Figure 1: BAC clone contigs spanning the SH3 locus. BAC clones spanning the SH3 locus as previously contigued [46]. Sequenced BACs from the three genomes are indicated by gray boxes.

Mentions: The sequences of a total of 13 BAC clones spanning the SH3 locus (Figure 1) in three coffee genomes (i.e. Ea and Ca sub-genome from C. arabica and Cc from C. canephora), were examined for the presence of R-genes using the previously determined annotation [48]. Depending on the genome concerned (Ea, Ca, Cc), a total of 5, 3 and 4 R-genes were identified, respectively. These sequences shared more than 95% of identity. According to Chen et al. [49], a R gene family is defined when 60% identity is shared by members. The R-gene sequences detected in SH3 were therefore further considered as members of a unique R-gene coffee family. BLAST analysis of the non-redundant database (All non-redundant GenBank CDS translations + RefSeq Proteins + PDB + SwissProt + PIR + PRF) revealed high similarity with several R-genes belonging to the CNL class. While the highest identity was observed with the hypothetical CNL R protein in Vitis vinifera (36% identity) in Ricinus communis and Glycine max (35%), the most similar functionally characterized protein was the RPP8 gene from Arabidopsis thaliana that confers resistance to Peronospora parasitica [36] and shares 32% of identity and more than 50% of similarity. Among the species belonging to the subclass Asteridae, which includes Coffea, several proteins where found in Solanum spp. which show 30% of identity and 50% of similarity with the R-gene family found at the SH3 locus of Coffea.


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

Ribas AF, Cenci A, Combes MC, Etienne H, Lashermes P - BMC Genomics (2011)

BAC clone contigs spanning the SH3 locus. BAC clones spanning the SH3 locus as previously contigued [46]. Sequenced BACs from the three genomes are indicated by gray boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3113787&req=5

Figure 1: BAC clone contigs spanning the SH3 locus. BAC clones spanning the SH3 locus as previously contigued [46]. Sequenced BACs from the three genomes are indicated by gray boxes.
Mentions: The sequences of a total of 13 BAC clones spanning the SH3 locus (Figure 1) in three coffee genomes (i.e. Ea and Ca sub-genome from C. arabica and Cc from C. canephora), were examined for the presence of R-genes using the previously determined annotation [48]. Depending on the genome concerned (Ea, Ca, Cc), a total of 5, 3 and 4 R-genes were identified, respectively. These sequences shared more than 95% of identity. According to Chen et al. [49], a R gene family is defined when 60% identity is shared by members. The R-gene sequences detected in SH3 were therefore further considered as members of a unique R-gene coffee family. BLAST analysis of the non-redundant database (All non-redundant GenBank CDS translations + RefSeq Proteins + PDB + SwissProt + PIR + PRF) revealed high similarity with several R-genes belonging to the CNL class. While the highest identity was observed with the hypothetical CNL R protein in Vitis vinifera (36% identity) in Ricinus communis and Glycine max (35%), the most similar functionally characterized protein was the RPP8 gene from Arabidopsis thaliana that confers resistance to Peronospora parasitica [36] and shares 32% of identity and more than 50% of similarity. Among the species belonging to the subclass Asteridae, which includes Coffea, several proteins where found in Solanum spp. which show 30% of identity and 50% of similarity with the R-gene family found at the SH3 locus of Coffea.

Bottom Line: All these R-gene sequences appeared to be members of a CC-NBS-LRR (CNL) gene family that was only found at the SH3 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.Gene conversion between paralog members, inter-subgenome sequence exchanges and positive selection appear to be the major forces acting on the evolution of SH3-CNL in coffee trees.

View Article: PubMed Central - HTML - PubMed

Affiliation: IRD - Institut de Recherche pour le Développement, UMR RPB, Montpellier Cedex, France.

ABSTRACT

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 SH3 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 SH3 locus.

Results: Sequence analysis of the SH3 region in three coffee genomes, Ea and Ca subgenomes from the allotetraploid C. arabica and Cc genome from the diploid C. canephora, revealed the presence of 5, 3 and 4 R genes in Ea, Ca, and Cc 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 SH3 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 SH3-CNL copies in the three analyzed genomes was determined and the duplication/deletion events that shaped the SH3 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 SH3-CNL copies.

Conclusion: The ancestral SH3-CNL copy was inserted in the SH3 locus after the divergence between Solanales and Rubiales lineages. Moreover, the origin of most of the SH3-CNL copies predates the divergence between Coffea species. The SH3-CNL family appeared to evolve following the birth-and-death model, since duplications and deletions were inferred in the evolution of the SH3 locus. Gene conversion between paralog members, inter-subgenome sequence exchanges and positive selection appear to be the major forces acting on the evolution of SH3-CNL in coffee trees.

Show MeSH
Related in: MedlinePlus