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Loss and retention of resistance genes in five species of the Brassicaceae family.

Peele HM, Guan N, Fogelqvist J, Dixelius C - BMC Plant Biol. (2014)

Bottom Line: On the contrary, the RLM3 locus important in the immune response towards Botrytis cinerea and Alternaria spp. has recently evolved in the Arabidopsis genus.Our genome-wide analysis of the R gene repertoire revealed a large sequence variation in the 23 cruciferous genomes.The data provides further insights into evolutionary processes impacting this important gene family.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Plants have evolved disease resistance (R) genes encoding for nucleotide-binding site (NB) and leucine-rich repeat (LRR) proteins with N-terminals represented by either Toll/Interleukin-1 receptor (TIR) or coiled-coil (CC) domains. Here, a genome-wide study of presence and diversification of CC-NB-LRR and TIR-NB-LRR encoding genes, and shorter domain combinations in 19 Arabidopsis thaliana accessions and Arabidopsis lyrata, Capsella rubella, Brassica rapa and Eutrema salsugineum are presented.

Results: Out of 528 R genes analyzed, 12 CC-NB-LRR and 17 TIR-NB-LRR genes were conserved among the 19 A. thaliana genotypes, while only two CC-NB-LRRs, including ZAR1, and three TIR-NB-LRRs were conserved when comparing the five species. The RESISTANCE TO LEPTOSPHAERIA MACULANS 1 (RLM1) locus confers resistance to the Brassica pathogen L. maculans the causal agent of blackleg disease and has undergone conservation and diversification events particularly in B. rapa. On the contrary, the RLM3 locus important in the immune response towards Botrytis cinerea and Alternaria spp. has recently evolved in the Arabidopsis genus.

Conclusion: Our genome-wide analysis of the R gene repertoire revealed a large sequence variation in the 23 cruciferous genomes. The data provides further insights into evolutionary processes impacting this important gene family.

No MeSH data available.


Related in: MedlinePlus

The TNL genes within theRLM1locus, TN genes in 19A. thalianaaccessions and theRLM3locus. In (A)p-distance of the different TNL encoding proteins in the RLM1 locus in the 19 A. thaliana accessions. Details on individual gene values see supporting information Additional file 9: Table S5. Domain architecture diversity of TIR-NB encoding R genes in 18 A. thaliana accessions in comparison with Col-0 with (B) total full-length or fragmented TIR-NB (TN) genes, and (C) distribution of 11 Col-0 TN proteins in 18 A. thaliana accessions. The genes encoding only a LRR are grouped with the absent genes. (D) Synteny in the RLM3 locus between A. thaliana Col-0, A. thaliana Kn-0, A. lyrata (Al), C. rubella (Cr), B. rapa (Br) and E. salsugineum (Es). *Early stop codon; **RLM3 locus in Rsch-4, Tsu-0, Wil-2, Ws-0 and Wu-0 are identical to Kn-0.
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Fig3: The TNL genes within theRLM1locus, TN genes in 19A. thalianaaccessions and theRLM3locus. In (A)p-distance of the different TNL encoding proteins in the RLM1 locus in the 19 A. thaliana accessions. Details on individual gene values see supporting information Additional file 9: Table S5. Domain architecture diversity of TIR-NB encoding R genes in 18 A. thaliana accessions in comparison with Col-0 with (B) total full-length or fragmented TIR-NB (TN) genes, and (C) distribution of 11 Col-0 TN proteins in 18 A. thaliana accessions. The genes encoding only a LRR are grouped with the absent genes. (D) Synteny in the RLM3 locus between A. thaliana Col-0, A. thaliana Kn-0, A. lyrata (Al), C. rubella (Cr), B. rapa (Br) and E. salsugineum (Es). *Early stop codon; **RLM3 locus in Rsch-4, Tsu-0, Wil-2, Ws-0 and Wu-0 are identical to Kn-0.

Mentions: Here, we found RLM1A to be present in all 18 A. thaliana accessions encoding all three domains in fourteen accessions (Can-0, Ct-1, Edi-0, Hi-0, Ler-0, Mt-0, No-0, Po-0, Sf-2, Tsu-0, Wil-2, Ws-0, Wu-0 and Zu-0 (Additional file 8: Table S4). This is in agreement with their resistance phenotype [29]. In general the RLM1A genes in 17 accessions had very few variable sites compared to RLM1A in Col-0 (p-distance 0.2 to 0.9%). Ws-0 was atypical and diverged most with 230 variable sites in comparison to RLM1A in Col-0 resulting in a p-distance of 13.8% (FigureĀ 3A and Additional file 9: Table S5). No RLM1A homologs were identified in the A. lyrata, B. rapa and E. salsugineum genomes. One RLM1A candidate was found un-annotated in the C. rubella genomic sequence and RNA expression data of the LRR region [30] suggests that this gene is expressed, and might have a potential role in defense responses. To support our findings, PCR amplification and sequencing of the RLM1A region in A. lyrata, B. rapa and C. rubella confirmed that only C. rubella has maintained RLM1A. B. rapa species are not known to host resistance to L. maculans [31] except the weedy relative B. rapa ssp. sylvestris [32,33]. In order to clarify the presence of RLM1A we used RLM1A specific primers to amplify this region in B. napus cv. Surpass 400 harboring resistance traits from the wild B. rapa relative, the gene progenitor, and for comparison, a known susceptible B. rapa genotype. Here, only B. rapa ssp. sylvestris contained a genomic sequence highly similar to the RLM1A gene of A. thaliana (identity 81%).Figure 3


Loss and retention of resistance genes in five species of the Brassicaceae family.

Peele HM, Guan N, Fogelqvist J, Dixelius C - BMC Plant Biol. (2014)

The TNL genes within theRLM1locus, TN genes in 19A. thalianaaccessions and theRLM3locus. In (A)p-distance of the different TNL encoding proteins in the RLM1 locus in the 19 A. thaliana accessions. Details on individual gene values see supporting information Additional file 9: Table S5. Domain architecture diversity of TIR-NB encoding R genes in 18 A. thaliana accessions in comparison with Col-0 with (B) total full-length or fragmented TIR-NB (TN) genes, and (C) distribution of 11 Col-0 TN proteins in 18 A. thaliana accessions. The genes encoding only a LRR are grouped with the absent genes. (D) Synteny in the RLM3 locus between A. thaliana Col-0, A. thaliana Kn-0, A. lyrata (Al), C. rubella (Cr), B. rapa (Br) and E. salsugineum (Es). *Early stop codon; **RLM3 locus in Rsch-4, Tsu-0, Wil-2, Ws-0 and Wu-0 are identical to Kn-0.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4232680&req=5

Fig3: The TNL genes within theRLM1locus, TN genes in 19A. thalianaaccessions and theRLM3locus. In (A)p-distance of the different TNL encoding proteins in the RLM1 locus in the 19 A. thaliana accessions. Details on individual gene values see supporting information Additional file 9: Table S5. Domain architecture diversity of TIR-NB encoding R genes in 18 A. thaliana accessions in comparison with Col-0 with (B) total full-length or fragmented TIR-NB (TN) genes, and (C) distribution of 11 Col-0 TN proteins in 18 A. thaliana accessions. The genes encoding only a LRR are grouped with the absent genes. (D) Synteny in the RLM3 locus between A. thaliana Col-0, A. thaliana Kn-0, A. lyrata (Al), C. rubella (Cr), B. rapa (Br) and E. salsugineum (Es). *Early stop codon; **RLM3 locus in Rsch-4, Tsu-0, Wil-2, Ws-0 and Wu-0 are identical to Kn-0.
Mentions: Here, we found RLM1A to be present in all 18 A. thaliana accessions encoding all three domains in fourteen accessions (Can-0, Ct-1, Edi-0, Hi-0, Ler-0, Mt-0, No-0, Po-0, Sf-2, Tsu-0, Wil-2, Ws-0, Wu-0 and Zu-0 (Additional file 8: Table S4). This is in agreement with their resistance phenotype [29]. In general the RLM1A genes in 17 accessions had very few variable sites compared to RLM1A in Col-0 (p-distance 0.2 to 0.9%). Ws-0 was atypical and diverged most with 230 variable sites in comparison to RLM1A in Col-0 resulting in a p-distance of 13.8% (FigureĀ 3A and Additional file 9: Table S5). No RLM1A homologs were identified in the A. lyrata, B. rapa and E. salsugineum genomes. One RLM1A candidate was found un-annotated in the C. rubella genomic sequence and RNA expression data of the LRR region [30] suggests that this gene is expressed, and might have a potential role in defense responses. To support our findings, PCR amplification and sequencing of the RLM1A region in A. lyrata, B. rapa and C. rubella confirmed that only C. rubella has maintained RLM1A. B. rapa species are not known to host resistance to L. maculans [31] except the weedy relative B. rapa ssp. sylvestris [32,33]. In order to clarify the presence of RLM1A we used RLM1A specific primers to amplify this region in B. napus cv. Surpass 400 harboring resistance traits from the wild B. rapa relative, the gene progenitor, and for comparison, a known susceptible B. rapa genotype. Here, only B. rapa ssp. sylvestris contained a genomic sequence highly similar to the RLM1A gene of A. thaliana (identity 81%).Figure 3

Bottom Line: On the contrary, the RLM3 locus important in the immune response towards Botrytis cinerea and Alternaria spp. has recently evolved in the Arabidopsis genus.Our genome-wide analysis of the R gene repertoire revealed a large sequence variation in the 23 cruciferous genomes.The data provides further insights into evolutionary processes impacting this important gene family.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Plants have evolved disease resistance (R) genes encoding for nucleotide-binding site (NB) and leucine-rich repeat (LRR) proteins with N-terminals represented by either Toll/Interleukin-1 receptor (TIR) or coiled-coil (CC) domains. Here, a genome-wide study of presence and diversification of CC-NB-LRR and TIR-NB-LRR encoding genes, and shorter domain combinations in 19 Arabidopsis thaliana accessions and Arabidopsis lyrata, Capsella rubella, Brassica rapa and Eutrema salsugineum are presented.

Results: Out of 528 R genes analyzed, 12 CC-NB-LRR and 17 TIR-NB-LRR genes were conserved among the 19 A. thaliana genotypes, while only two CC-NB-LRRs, including ZAR1, and three TIR-NB-LRRs were conserved when comparing the five species. The RESISTANCE TO LEPTOSPHAERIA MACULANS 1 (RLM1) locus confers resistance to the Brassica pathogen L. maculans the causal agent of blackleg disease and has undergone conservation and diversification events particularly in B. rapa. On the contrary, the RLM3 locus important in the immune response towards Botrytis cinerea and Alternaria spp. has recently evolved in the Arabidopsis genus.

Conclusion: Our genome-wide analysis of the R gene repertoire revealed a large sequence variation in the 23 cruciferous genomes. The data provides further insights into evolutionary processes impacting this important gene family.

No MeSH data available.


Related in: MedlinePlus