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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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Related in: MedlinePlus

Southern blot hybridization of genomic DNA of C. Arabica. DNA from the IAPAR-59 accession was digested with EcoRI, DraI and BamHI enzymes. The probe corresponded to the part of the NBS region that is highlighted by a frame in figure 6.
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Figure 3: Southern blot hybridization of genomic DNA of C. Arabica. DNA from the IAPAR-59 accession was digested with EcoRI, DraI and BamHI enzymes. The probe corresponded to the part of the NBS region that is highlighted by a frame in figure 6.

Mentions: To test for the presence of a possible additional copy of the SH3-CNL in the Arabica coffee genome, Southern blot analysis was performed using a specific probe corresponding to a conserved part of the NBS region (Figure 3). Whatever the restriction enzyme used, only a limited number of hybridization bands was detected. Based on the restriction profiles predicted from sequence analysis of C. arabica cv. IAPAR-59 BAC, it was possible to assign all the bands to one of the eight members (five in the Ea genome and three in the Ca genome) present at the SH3 locus. No additional band was detected, suggesting that this family is only present at the SH3 locus in C. arabica cv. IAPAR-59. In fact, even if it is possible that additional hybridization fragments have size out of the detectable range, this should happened for all the three restriction enzymes and can be considered as a very improbable event.


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)

Southern blot hybridization of genomic DNA of C. Arabica. DNA from the IAPAR-59 accession was digested with EcoRI, DraI and BamHI enzymes. The probe corresponded to the part of the NBS region that is highlighted by a frame in figure 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Southern blot hybridization of genomic DNA of C. Arabica. DNA from the IAPAR-59 accession was digested with EcoRI, DraI and BamHI enzymes. The probe corresponded to the part of the NBS region that is highlighted by a frame in figure 6.
Mentions: To test for the presence of a possible additional copy of the SH3-CNL in the Arabica coffee genome, Southern blot analysis was performed using a specific probe corresponding to a conserved part of the NBS region (Figure 3). Whatever the restriction enzyme used, only a limited number of hybridization bands was detected. Based on the restriction profiles predicted from sequence analysis of C. arabica cv. IAPAR-59 BAC, it was possible to assign all the bands to one of the eight members (five in the Ea genome and three in the Ca genome) present at the SH3 locus. No additional band was detected, suggesting that this family is only present at the SH3 locus in C. arabica cv. IAPAR-59. In fact, even if it is possible that additional hybridization fragments have size out of the detectable range, this should happened for all the three restriction enzymes and can be considered as a very improbable event.

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