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Distinct Evolutionary Patterns of NBS-Encoding Genes in Three Soapberry Family (Sapindaceae) Species.

ABSTRACT: Nucleotide-binding site (NBS)-type disease resistance genes (R genes) play key roles in plant immune responses and have co-evolved with pathogens over the course of plant lifecycles. Comparative genomic studies tracing the dynamic evolution of NBS-encoding genes have been conducted using many important plant lineages. However, studies on Sapindaceae species have not been performed. In this study, a discrepant number of NBS-encoding genes were identified in the genomes of Xanthoceras sorbifolium (180), Dinnocarpus longan (568), and Acer yangbiense (252). These genes were unevenly distributed and usually clustered as tandem arrays on chromosomes, with few existed as singletons. The phylogenetic analysis revealed that NBS-encoding genes formed three monophyletic clades, RPW8-NBS-LRR (RNL), TIR-NBS-LRR (TNL), and CC-NBS-LRR (CNL), which were distinguished by amino acid motifs. The NBS-encoding genes of the X. sorbifolium, D. longan, and A. yangbiense genomes were derived from 181 ancestral genes (three RNL, 23 TNL, and 155 CNL), which exhibited dynamic and distinct evolutionary patterns due to independent gene duplication/loss events. Specifically, X. sorbifolium exhibited a "first expansion and then contraction" evolutionary pattern, while A. yangbiense and D. longan exhibited a "first expansion followed by contraction and further expansion" evolutionary pattern. However, further expansion in D. longan was stronger than in A. yangbiense after divergence, suggesting that D. longan gained more genes in response to various pathogens. Additionally, the ancient and recent expansion of CNL genes generated the dominance of this subclass in terms of gene numbers, while the low copy number status of RNL genes was attributed to their conserved functions.

SUBMITTER: Zhou GC

PROVIDER: S-EPMC7365912 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundNucleotide binding site (NBS) genes encode a large family of disease resistance (R) proteins in plants. The availability of genomic data of the two diploid cotton species, Gossypium arboreum and Gossypium raimondii, and the two allotetraploid cotton species, Gossypium hirsutum (TM-1) and Gossypium barbadense allow for a more comprehensive and systematic comparative study of NBS-encoding genes to elucidate the mechanisms of cotton disease resistance.ResultsBased on the genome assembly data, 246, 365, 588 and 682 NBS-encoding genes were identified in G. arboreum, G. raimondii, G. hirsutum and G. barbadense, respectively. The distribution of NBS-encoding genes among the chromosomes was nonrandom and uneven, and was tended to form clusters. Gene structure analysis showed that G. arboreum and G. hirsutum possessed a greater proportion of CN, CNL, and N genes and a lower proportion of NL, TN and TNL genes compared to that of G. raimondii and G. barbadense, while the percentages of RN and RNL genes remained relatively unchanged. The percentage changes among them were largest for TNL genes, about 7 times. Exon statistics showed that the average exon numbers per NBS gene in G. raimondii and G. barbadense were all greater than that in G. arboretum and G. hirsutum. Phylogenetic analysis revealed that the TIR-NBS genes of G. barbadense were closely related with that of G. raimondii. Sequence similarity analysis showed that diploid cotton G. arboreum possessed a larger proportion of NBS-encoding genes similar to that of allotetraploid cotton G. hirsutum, while diploid G. raimondii possessed a larger proportion of NBS-encoding genes similar to that of allotetraploid cotton G. barbadense. The synteny analysis showed that more NBS genes in G. raimondii and G. arboreum were syntenic with that in G. barbadense and G. hirsutum, respectively.ConclusionsThe structural architectures, amino acid sequence similarities and synteny of NBS-encoding genes between G. arboreum and G. hirsutum, and between G. raimondii and G. barbadense were the highest among comparisons between the diploid and allotetraploid genomes, indicating that G. hirsutum inherited more NBS-encoding genes from G. arboreum, while G. barbadense inherited more NBS-encoding genes from G. raimondii. This asymmetric evolution of NBS-encoding genes may help to explain why G. raimondii and G. barbadense are more resistant to Verticillium wilt, whereas G. arboreum and G. hirsutum are more susceptible to Verticillium wilt. The disease resistances of the allotetraploid cotton were related to their NBS-encoding genes especially in regard from which diploid progenitor they were derived, and the TNL genes may have a significant role in disease resistance to Verticillium wilt in G. raimondii and G. barbadense.

Project description:BACKGROUND: Plant disease resistance (R) genes with the nucleotide binding site (NBS) play an important role in offering resistance to pathogens. The availability of complete genome sequences of Brassica oleracea and Brassica rapa provides an important opportunity for researchers to identify and characterize NBS-encoding R genes in Brassica species and to compare with analogues in Arabidopsis thaliana based on a comparative genomics approach. However, little is known about the evolutionary fate of NBS-encoding genes in the Brassica lineage after split from A. thaliana. RESULTS: Here we present genome-wide analysis of NBS-encoding genes in B. oleracea, B. rapa and A. thaliana. Through the employment of HMM search and manual curation, we identified 157, 206 and 167 NBS-encoding genes in B. oleracea, B. rapa and A. thaliana genomes, respectively. Phylogenetic analysis among 3 species classified NBS-encoding genes into 6 subgroups. Tandem duplication and whole genome triplication (WGT) analyses revealed that after WGT of the Brassica ancestor, NBS-encoding homologous gene pairs on triplicated regions in Brassica ancestor were deleted or lost quickly, but NBS-encoding genes in Brassica species experienced species-specific gene amplification by tandem duplication after divergence of B. rapa and B. oleracea. Expression profiling of NBS-encoding orthologous gene pairs indicated the differential expression pattern of retained orthologous gene copies in B. oleracea and B. rapa. Furthermore, evolutionary analysis of CNL type NBS-encoding orthologous gene pairs among 3 species suggested that orthologous genes in B. rapa species have undergone stronger negative selection than those in B .oleracea species. But for TNL type, there are no significant differences in the orthologous gene pairs between the two species. CONCLUSION: This study is first identification and characterization of NBS-encoding genes in B. rapa and B. oleracea based on whole genome sequences. Through tandem duplication and whole genome triplication analysis in B. oleracea, B. rapa and A. thaliana genomes, our study provides insight into the evolutionary history of NBS-encoding genes after divergence of A. thaliana and the Brassica lineage. These results together with expression pattern analysis of NBS-encoding orthologous genes provide useful resource for functional characterization of these genes and genetic improvement of relevant crops.

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Distinct Evolutionary Patterns of NBS-Encoding Genes in Three Soapberry Family (Sapindaceae) Species.

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