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

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, b...

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Autores principales: Sun, Manyi, Zhang, Mingyue, Singh, Jugpreet, Song, Bobo, Tang, Zikai, Liu, Yueyuan, Wang, Runze, Qin, Mengfan, Li, Jiaming, Khan, Awais, Wu, Jun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7678159/
https://www.ncbi.nlm.nih.gov/pubmed/33213380
http://dx.doi.org/10.1186/s12864-020-07226-1
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author Sun, Manyi
Zhang, Mingyue
Singh, Jugpreet
Song, Bobo
Tang, Zikai
Liu, Yueyuan
Wang, Runze
Qin, Mengfan
Li, Jiaming
Khan, Awais
Wu, Jun
author_facet Sun, Manyi
Zhang, Mingyue
Singh, Jugpreet
Song, Bobo
Tang, Zikai
Liu, Yueyuan
Wang, Runze
Qin, Mengfan
Li, Jiaming
Khan, Awais
Wu, Jun
author_sort Sun, Manyi
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07226-1.
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spelling pubmed-76781592020-11-20 Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears Sun, Manyi Zhang, Mingyue Singh, Jugpreet Song, Bobo Tang, Zikai Liu, Yueyuan Wang, Runze Qin, Mengfan Li, Jiaming Khan, Awais Wu, Jun BMC Genomics Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-020-07226-1. BioMed Central 2020-11-19 /pmc/articles/PMC7678159/ /pubmed/33213380 http://dx.doi.org/10.1186/s12864-020-07226-1 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Sun, Manyi
Zhang, Mingyue
Singh, Jugpreet
Song, Bobo
Tang, Zikai
Liu, Yueyuan
Wang, Runze
Qin, Mengfan
Li, Jiaming
Khan, Awais
Wu, Jun
Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7678159/
https://www.ncbi.nlm.nih.gov/pubmed/33213380
http://dx.doi.org/10.1186/s12864-020-07226-1
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