Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication

Abstract Background Persian walnut, Juglans regia, occurs naturally from Greece to western China, while its closest relative, the iron walnut, Juglans sigillata, is endemic in southwest China; both species are cultivated for their nuts and wood. Here, we infer their demographic histories and the tim...

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Main Authors: Ya-Mei Ding, Yu Cao, Wei-Ping Zhang, Jun Chen, Jie Liu, Pan Li, Susanne S. Renner, Da-Yong Zhang, Wei-Ning Bai
Format: Article
Language:English
Published: BMC 2022-07-01
Series:Genome Biology
Subjects:
Online Access:https://doi.org/10.1186/s13059-022-02720-z
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author Ya-Mei Ding
Yu Cao
Wei-Ping Zhang
Jun Chen
Jie Liu
Pan Li
Susanne S. Renner
Da-Yong Zhang
Wei-Ning Bai
author_facet Ya-Mei Ding
Yu Cao
Wei-Ping Zhang
Jun Chen
Jie Liu
Pan Li
Susanne S. Renner
Da-Yong Zhang
Wei-Ning Bai
author_sort Ya-Mei Ding
collection DOAJ
description Abstract Background Persian walnut, Juglans regia, occurs naturally from Greece to western China, while its closest relative, the iron walnut, Juglans sigillata, is endemic in southwest China; both species are cultivated for their nuts and wood. Here, we infer their demographic histories and the time and direction of possible hybridization and introgression between them. Results We use whole-genome resequencing data, different population-genetic approaches (PSMC and GONE), and isolation-with-migration models (IMa3) on individuals from Europe, Iran, Kazakhstan, Pakistan, and China. IMa3 analyses indicate that the two species diverged from each other by 0.85 million years ago, with unidirectional gene flow from eastern J. regia and its ancestor into J. sigillata, including the shell-thickness gene. Within J. regia, a western group, located from Europe to Iran, and an eastern group with individuals from northern China, experienced dramatically declining population sizes about 80 generations ago (roughly 2400 to 4000 years), followed by an expansion at about 40 generations, while J. sigillata had a constant population size from about 100 to 20 generations ago, followed by a rapid decline. Conclusions Both J. regia and J. sigillata appear to have suffered sudden population declines during their domestication, suggesting that the bottleneck scenario of plant domestication may well apply in at least some perennial crop species. Introgression from introduced J. regia appears to have played a role in the domestication of J. sigillata.
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spelling doaj.art-391f0a1b57c040f8b89274ec57224e052022-12-22T02:44:11ZengBMCGenome Biology1474-760X2022-07-0123111810.1186/s13059-022-02720-zPopulation-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domesticationYa-Mei Ding0Yu Cao1Wei-Ping Zhang2Jun Chen3Jie Liu4Pan Li5Susanne S. Renner6Da-Yong Zhang7Wei-Ning Bai8State Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityState Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityState Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityState Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesThe Key Laboratory of Conservation Biology for Endangered Wildlife of the Ministry of Education, College of Life Sciences, Zhejiang UniversityDepartment of Biology, Washington UniversityState Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityState Key Laboratory of Earth Surface Processes and Resource Ecology and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal UniversityAbstract Background Persian walnut, Juglans regia, occurs naturally from Greece to western China, while its closest relative, the iron walnut, Juglans sigillata, is endemic in southwest China; both species are cultivated for their nuts and wood. Here, we infer their demographic histories and the time and direction of possible hybridization and introgression between them. Results We use whole-genome resequencing data, different population-genetic approaches (PSMC and GONE), and isolation-with-migration models (IMa3) on individuals from Europe, Iran, Kazakhstan, Pakistan, and China. IMa3 analyses indicate that the two species diverged from each other by 0.85 million years ago, with unidirectional gene flow from eastern J. regia and its ancestor into J. sigillata, including the shell-thickness gene. Within J. regia, a western group, located from Europe to Iran, and an eastern group with individuals from northern China, experienced dramatically declining population sizes about 80 generations ago (roughly 2400 to 4000 years), followed by an expansion at about 40 generations, while J. sigillata had a constant population size from about 100 to 20 generations ago, followed by a rapid decline. Conclusions Both J. regia and J. sigillata appear to have suffered sudden population declines during their domestication, suggesting that the bottleneck scenario of plant domestication may well apply in at least some perennial crop species. Introgression from introduced J. regia appears to have played a role in the domestication of J. sigillata.https://doi.org/10.1186/s13059-022-02720-zDomestication bottleneckIntrogressionIron walnutPersian walnutShell-thickness gene
spellingShingle Ya-Mei Ding
Yu Cao
Wei-Ping Zhang
Jun Chen
Jie Liu
Pan Li
Susanne S. Renner
Da-Yong Zhang
Wei-Ning Bai
Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
Genome Biology
Domestication bottleneck
Introgression
Iron walnut
Persian walnut
Shell-thickness gene
title Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
title_full Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
title_fullStr Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
title_full_unstemmed Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
title_short Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication
title_sort population genomic analyses reveal bottlenecks and asymmetric introgression from persian into iron walnut during domestication
topic Domestication bottleneck
Introgression
Iron walnut
Persian walnut
Shell-thickness gene
url https://doi.org/10.1186/s13059-022-02720-z
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