Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears

Abstract Background The NBS disease-related gene family coordinates the inherent immune system in plants in response to pathogen infections. Previous studies have identified NBS-encoding genes in Pyrus bretschneideri (‘Dangshansuli’, an Asian pear) and Pyrus communis (‘Bartlett’, a European pear) ge...

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Main Authors: Manyi Sun, Mingyue Zhang, Jugpreet Singh, Bobo Song, Zikai Tang, Yueyuan Liu, Runze Wang, Mengfan Qin, Jiaming Li, Awais Khan, Jun Wu
Format: Article
Language:English
Published: BMC 2020-11-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-07226-1
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author Manyi Sun
Mingyue Zhang
Jugpreet Singh
Bobo Song
Zikai Tang
Yueyuan Liu
Runze Wang
Mengfan Qin
Jiaming Li
Awais Khan
Jun Wu
author_facet Manyi Sun
Mingyue Zhang
Jugpreet Singh
Bobo Song
Zikai Tang
Yueyuan Liu
Runze Wang
Mengfan Qin
Jiaming Li
Awais Khan
Jun Wu
author_sort Manyi Sun
collection DOAJ
description Abstract Background The NBS disease-related gene family coordinates the inherent immune system in plants in response to pathogen infections. Previous studies have identified NBS-encoding genes in Pyrus bretschneideri (‘Dangshansuli’, an Asian pear) and Pyrus communis (‘Bartlett’, a European pear) genomes, but the patterns of genetic variation and selection pressure on these genes during pear domestication have remained unsolved. Results In this study, 338 and 412 NBS-encoding genes were identified from Asian and European pear genomes. This difference between the two pear species was the result of proximal duplications. About 15.79% orthologous gene pairs had Ka/Ks ratio more than one, indicating two pear species undergo strong positive selection after the divergence of Asian and European pear. We identified 21 and 15 NBS-encoding genes under fire blight and black spot disease-related QTL, respectively, suggesting their importance in disease resistance. Domestication caused decreased nucleotide diversity across NBS genes in Asian cultivars (cultivated 6.23E-03; wild 6.47E-03), but opposite trend (cultivated 6.48E-03; wild 5.91E-03) appeared in European pears. Many NBS-encoding coding regions showed Ka/Ks ratio of greater than 1, indicating the role of positive selection in shaping diversity of NBS-encoding genes in pear. Furthermore, we detected 295 and 122 significantly different SNPs between wild and domesticated accessions in Asian and European pear populations. Two NBS genes (Pbr025269.1 and Pbr019876.1) with significantly different SNPs showed >5x upregulation between wild and cultivated pear accessions, and > 2x upregulation in Pyrus calleryana after inoculation with Alternaria alternata. We propose that positively selected and significantly different SNPs of an NBS-encoding gene (Pbr025269.1) regulate gene expression differences in the wild and cultivated groups, which may affect resistance in pear against A. alternata. Conclusion Proximal duplication mainly led to the different number of NBS-encoding genes in P. bretschneideri and P. communis genomes. The patterns of genetic diversity and positive selection pressure differed between Asian and European pear populations, most likely due to their independent domestication events. This analysis helps us understand the evolution, diversity, and selection pressure in the NBS-encoding gene family in Asian and European populations, and provides opportunities to study mechanisms of disease resistance in pear.
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spelling doaj.art-6a29f08b85634f9e831ca3f0d88cdc482022-12-22T00:56:39ZengBMCBMC Genomics1471-21642020-11-0121111610.1186/s12864-020-07226-1Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pearsManyi Sun0Mingyue Zhang1Jugpreet Singh2Bobo Song3Zikai Tang4Yueyuan Liu5Runze Wang6Mengfan Qin7Jiaming Li8Awais Khan9Jun Wu10College of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityPlant Pathology & Plant-Microbe Biology Section, Cornell UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityPlant Pathology & Plant-Microbe Biology Section, Cornell UniversityCollege of Horticulture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural UniversityAbstract Background The NBS disease-related gene family coordinates the inherent immune system in plants in response to pathogen infections. Previous studies have identified NBS-encoding genes in Pyrus bretschneideri (‘Dangshansuli’, an Asian pear) and Pyrus communis (‘Bartlett’, a European pear) genomes, but the patterns of genetic variation and selection pressure on these genes during pear domestication have remained unsolved. Results In this study, 338 and 412 NBS-encoding genes were identified from Asian and European pear genomes. This difference between the two pear species was the result of proximal duplications. About 15.79% orthologous gene pairs had Ka/Ks ratio more than one, indicating two pear species undergo strong positive selection after the divergence of Asian and European pear. We identified 21 and 15 NBS-encoding genes under fire blight and black spot disease-related QTL, respectively, suggesting their importance in disease resistance. Domestication caused decreased nucleotide diversity across NBS genes in Asian cultivars (cultivated 6.23E-03; wild 6.47E-03), but opposite trend (cultivated 6.48E-03; wild 5.91E-03) appeared in European pears. Many NBS-encoding coding regions showed Ka/Ks ratio of greater than 1, indicating the role of positive selection in shaping diversity of NBS-encoding genes in pear. Furthermore, we detected 295 and 122 significantly different SNPs between wild and domesticated accessions in Asian and European pear populations. Two NBS genes (Pbr025269.1 and Pbr019876.1) with significantly different SNPs showed >5x upregulation between wild and cultivated pear accessions, and > 2x upregulation in Pyrus calleryana after inoculation with Alternaria alternata. We propose that positively selected and significantly different SNPs of an NBS-encoding gene (Pbr025269.1) regulate gene expression differences in the wild and cultivated groups, which may affect resistance in pear against A. alternata. Conclusion Proximal duplication mainly led to the different number of NBS-encoding genes in P. bretschneideri and P. communis genomes. The patterns of genetic diversity and positive selection pressure differed between Asian and European pear populations, most likely due to their independent domestication events. This analysis helps us understand the evolution, diversity, and selection pressure in the NBS-encoding gene family in Asian and European populations, and provides opportunities to study mechanisms of disease resistance in pear.http://link.springer.com/article/10.1186/s12864-020-07226-1NBSPearExpansionPositive selectionNucleotide diversity
spellingShingle Manyi Sun
Mingyue Zhang
Jugpreet Singh
Bobo Song
Zikai Tang
Yueyuan Liu
Runze Wang
Mengfan Qin
Jiaming Li
Awais Khan
Jun Wu
Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
BMC Genomics
NBS
Pear
Expansion
Positive selection
Nucleotide diversity
title Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
title_full Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
title_fullStr Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
title_full_unstemmed Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
title_short Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
title_sort contrasting genetic variation and positive selection followed the divergence of nbs encoding genes in asian and european pears
topic NBS
Pear
Expansion
Positive selection
Nucleotide diversity
url http://link.springer.com/article/10.1186/s12864-020-07226-1
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