Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance

Abstract Background The nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes are important for plant development and disease resistance. Although genome-wide studies of NBS-encoding genes have been performed in several species, the evolution, structure, expression, and function of these genes...

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Main Authors: Yinbo Ma, Sushil Satish Chhapekar, Lu Lu, Sangheon Oh, Sonam Singh, Chang Soo Kim, Seungho Kim, Gyung Ja Choi, Yong Pyo Lim, Su Ryun Choi
Format: Article
Language:English
Published: BMC 2021-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-020-02803-8
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author Yinbo Ma
Sushil Satish Chhapekar
Lu Lu
Sangheon Oh
Sonam Singh
Chang Soo Kim
Seungho Kim
Gyung Ja Choi
Yong Pyo Lim
Su Ryun Choi
author_facet Yinbo Ma
Sushil Satish Chhapekar
Lu Lu
Sangheon Oh
Sonam Singh
Chang Soo Kim
Seungho Kim
Gyung Ja Choi
Yong Pyo Lim
Su Ryun Choi
author_sort Yinbo Ma
collection DOAJ
description Abstract Background The nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes are important for plant development and disease resistance. Although genome-wide studies of NBS-encoding genes have been performed in several species, the evolution, structure, expression, and function of these genes remain unknown in radish (Raphanus sativus L.). A recently released draft R. sativus L. reference genome has facilitated the genome-wide identification and characterization of NBS-encoding genes in radish. Results A total of 225 NBS-encoding genes were identified in the radish genome based on the essential NB-ARC domain through HMM search and Pfam database, with 202 mapped onto nine chromosomes and the remaining 23 localized on different scaffolds. According to a gene structure analysis, we identified 99 NBS-LRR-type genes and 126 partial NBS-encoding genes. Additionally, 80 and 19 genes respectively encoded an N-terminal Toll/interleukin-like domain and a coiled-coil domain. Furthermore, 72% of the 202 NBS-encoding genes were grouped in 48 clusters distributed in 24 crucifer blocks on chromosomes. The U block on chromosomes R02, R04, and R08 had the most NBS-encoding genes (48), followed by the R (24), D (23), E (23), and F (17) blocks. These clusters were mostly homogeneous, containing NBS-encoding genes derived from a recent common ancestor. Tandem (15 events) and segmental (20 events) duplications were revealed in the NBS family. Comparative evolutionary analyses of orthologous genes among Arabidopsis thaliana, Brassica rapa, and Brassica oleracea reflected the importance of the NBS-LRR gene family during evolution. Moreover, examinations of cis-elements identified 70 major elements involved in responses to methyl jasmonate, abscisic acid, auxin, and salicylic acid. According to RNA-seq expression analyses, 75 NBS-encoding genes contributed to the resistance of radish to Fusarium wilt. A quantitative real-time PCR analysis revealed that RsTNL03 (Rs093020) and RsTNL09 (Rs042580) expression positively regulates radish resistance to Fusarium oxysporum, in contrast to the negative regulatory role for RsTNL06 (Rs053740). Conclusions The NBS-encoding gene structures, tandem and segmental duplications, synteny, and expression profiles in radish were elucidated for the first time and compared with those of other Brassicaceae family members (A. thaliana, B. oleracea, and B. rapa) to clarify the evolution of the NBS gene family. These results may be useful for functionally characterizing NBS-encoding genes in radish.
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spelling doaj.art-16e735741ad2487f813b9d7aa17fa0622022-12-21T23:23:32ZengBMCBMC Plant Biology1471-22292021-01-0121111710.1186/s12870-020-02803-8Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistanceYinbo Ma0Sushil Satish Chhapekar1Lu Lu2Sangheon Oh3Sonam Singh4Chang Soo Kim5Seungho Kim6Gyung Ja Choi7Yong Pyo Lim8Su Ryun Choi9Molecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityDepartment of Crop Science, College of Agricultural and Life Sciences, Chungnam National UniversityNeo Seed Co.Center for Eco-friendly New Materials, Korea Research Institute of Chemical TechnologyMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityMolecular Genetics and Genomics Laboratory, Department of Horticulture, College of Agriculture and Life Science, Chungnam National UniversityAbstract Background The nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes are important for plant development and disease resistance. Although genome-wide studies of NBS-encoding genes have been performed in several species, the evolution, structure, expression, and function of these genes remain unknown in radish (Raphanus sativus L.). A recently released draft R. sativus L. reference genome has facilitated the genome-wide identification and characterization of NBS-encoding genes in radish. Results A total of 225 NBS-encoding genes were identified in the radish genome based on the essential NB-ARC domain through HMM search and Pfam database, with 202 mapped onto nine chromosomes and the remaining 23 localized on different scaffolds. According to a gene structure analysis, we identified 99 NBS-LRR-type genes and 126 partial NBS-encoding genes. Additionally, 80 and 19 genes respectively encoded an N-terminal Toll/interleukin-like domain and a coiled-coil domain. Furthermore, 72% of the 202 NBS-encoding genes were grouped in 48 clusters distributed in 24 crucifer blocks on chromosomes. The U block on chromosomes R02, R04, and R08 had the most NBS-encoding genes (48), followed by the R (24), D (23), E (23), and F (17) blocks. These clusters were mostly homogeneous, containing NBS-encoding genes derived from a recent common ancestor. Tandem (15 events) and segmental (20 events) duplications were revealed in the NBS family. Comparative evolutionary analyses of orthologous genes among Arabidopsis thaliana, Brassica rapa, and Brassica oleracea reflected the importance of the NBS-LRR gene family during evolution. Moreover, examinations of cis-elements identified 70 major elements involved in responses to methyl jasmonate, abscisic acid, auxin, and salicylic acid. According to RNA-seq expression analyses, 75 NBS-encoding genes contributed to the resistance of radish to Fusarium wilt. A quantitative real-time PCR analysis revealed that RsTNL03 (Rs093020) and RsTNL09 (Rs042580) expression positively regulates radish resistance to Fusarium oxysporum, in contrast to the negative regulatory role for RsTNL06 (Rs053740). Conclusions The NBS-encoding gene structures, tandem and segmental duplications, synteny, and expression profiles in radish were elucidated for the first time and compared with those of other Brassicaceae family members (A. thaliana, B. oleracea, and B. rapa) to clarify the evolution of the NBS gene family. These results may be useful for functionally characterizing NBS-encoding genes in radish.https://doi.org/10.1186/s12870-020-02803-8Raphanus sativus L.NBS-encoding geneGene duplicationEvolutionSyntenyFusarium oxysporum
spellingShingle Yinbo Ma
Sushil Satish Chhapekar
Lu Lu
Sangheon Oh
Sonam Singh
Chang Soo Kim
Seungho Kim
Gyung Ja Choi
Yong Pyo Lim
Su Ryun Choi
Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
BMC Plant Biology
Raphanus sativus L.
NBS-encoding gene
Gene duplication
Evolution
Synteny
Fusarium oxysporum
title Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
title_full Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
title_fullStr Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
title_full_unstemmed Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
title_short Genome-wide identification and characterization of NBS-encoding genes in Raphanus sativus L. and their roles related to Fusarium oxysporum resistance
title_sort genome wide identification and characterization of nbs encoding genes in raphanus sativus l and their roles related to fusarium oxysporum resistance
topic Raphanus sativus L.
NBS-encoding gene
Gene duplication
Evolution
Synteny
Fusarium oxysporum
url https://doi.org/10.1186/s12870-020-02803-8
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