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Title: Genome-wide comparative analysis reveals similar types of NBS genes in hybrid Citrus sinensis genome and original Citrus clementine genome and provides new insights into non-TIR NBS genes

Author
item WANG, YUN SHEN - Clemson University
item ZHOU, LIJUAN - University Of Florida
item LI, DAZHI - Hunan Agricultural University
item DAI, LIANGYING - Hunan Agricultural University
item LAWTON-RAUH, AMY - Clemson University
item SRIMANI, PRADIP - Clemson University
item Duan, Ping
item LOU, FENG - Clemson University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2015
Publication Date: 3/26/2015
Citation: Wang, Y., Zhou, L., Li, D., Dai, L., Lawton-Rauh, A., Srimani, P.K., Duan, Y., Lou, F. 2015. Genome-wide comparative analysis reveals similar types of NBS genes in hybrid Citrus sinensis genome and original Citrus clementine genome and provides new insights into non-TIR NBS genes. PLoS One. 10(3):e0121893. doi: 10.1371.

Interpretive Summary: Disease resistance genes (R genes) are essential components of plant immune systems. Amongst five diverse classes of disease resistance genes, the largest class of R genes includes genes that encode proteins with a nucleotide-binding site (NBS) domain and a Leucine-Rich Repeat (LRR) domain. The NBS domain is highly sequence constrained and is typically used to identify and characterize plant R genes. Genome-wide analyses of NBS genes in many genomes have shown that NBS R genes are diverse in number, structure and organization. Citrus species are amongst the most important fruit trees and have been cultivated for more than 4000 years. Recently available draft whole genome sequences of three Citrus species: C. clementina, C. sinensis from USA and C. sinensis from China, have made it possible to scan and identify all NBS genes in those genomes. In this study, we performed a genome-wide comparative analysis of NBS genes in three Citrus genomes (C. clementina, C. sinensis from China and C. sinensis from USA). Phylogenetic analysis of all Citrus NBS genes across these three genomes revealed that there are three approximately evenly numbered groups: one group contains the Toll-Interleukin receptor (TIR) domain and two different Non-TIR groups in which most of proteins contain the Coiled Coil (CC) domain. Motif analysis confirmed that the two groups of CC-containing NBS genes are from different evolutionary origins. We partitioned NBS genes into clades using NBS domain sequence distances and found most clades include NBS genes from all three Citrus genomes. This suggests that three Citrus genomes have similar numbers and types of NBS genes. We also mapped the re-sequenced reads of three pomelo and three mandarin genomes onto the C. sinensis genome. We found that most NBS genes of the hybrid C. sinensis genome have corresponding homologous genes in both pomelo and mandarin genomes. The homologous NBS genes in pomelo and mandarin suggest that the parental species of C. sinensis may contain similar types of NBS genes. This explains why the hybrid C. sinensis and original C. clementina have similar types of NBS genes in this study. Furthermore, we found that sequence variation amongst Citrus NBS genes were shaped by multiple independent and shared accelerated mutation accumulation events among different groups of NBS genes and in different Citrus genomes. Our comparative analyses yield valuable insight into the structure, organization and evolution of NBS genes in Citrus genomes.

Technical Abstract: In this study, we identified and compared nucleotide-binding site (NBS) domain-containing genes from three Citrus genomes (C. clementina, C. sinensis from USA and C. sinensis from China). Phylogenetic analysis of all Citrus NBS genes across these three genomes revealed that there are three approximately evenly numbered groups: one group contains the Toll-Interleukin receptor (TIR) domain and two different Non-TIR groups in which most of proteins contain the Coiled Coil (CC) domain. Motif analysis confirmed that the two groups of CC-containing NBS genes are from different evolutionary origins. We partitioned NBS genes into clades using NBS domain sequence distances and found most clades include NBS genes from all three Citrus genomes. This suggests that three Citrus genomes have similar numbers and types of NBS genes. We also mapped the re-sequenced reads of three pomelo and three mandarin genomes onto the C. sinensis genome. We found that most NBS genes of the hybrid C. sinensis genome have corresponding homologous genes in both pomelo and mandarin genomes. The homologous NBS genes in pomelo and mandarin suggest that the parental species of C. sinensis may contain similar types of NBS genes. This explains why the hybrid C. sinensis and original C. clementina have similar types of NBS genes in this study. Furthermore, we found that sequence variation amongst Citrus NBS genes were shaped by multiple independent and shared accelerated mutation accumulation events among different groups of NBS genes and in different Citrus genomes. Our comparative analyses yield valuable insight into the structure, organization and evolution of NBS genes in Citrus genomes. Furthermore, our comprehensive analysis showed that the non-TIR NBS genes can be divided into two groups that come from different evolutionary origins. This provides new insights into non- TIR genes, which have not received much attention.