Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization

Li-Jun Yan; Peng-Zhen Fan; Moses C Wambulwa; Hai-Ling Qi; Ying Chen; Zeng-Yuan Wu; Richard I. Milne; Raees Khan; Ya-Huang Luo; Lian-Ming Gao; Shi-Kang  Shen; Irfan  Rashid; Shujaul Mulk  Khan; Debabrata Maity; De-Zhu Li; Jie Liu

doi:10.1111/ddi.13809

Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization

Li-Jun Yan, Peng-Zhen Fan, Moses C Wambulwa, Hai-Ling Qi, Ying Chen, Zeng-Yuan Wu, Richard I. Milne, Raees Khan, Ya-Huang Luo, Lian-Ming Gao, Shi-Kang Shen, Irfan Rashid, Shujaul Mulk Khan, Debabrata Maity, De-Zhu Li, Jie Liu

School of Biological Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Aims: A comprehensive understanding of the genetic variation of walnuts (Juglans regia and J. sigillata) in the Himalaya and its potential drivers are essential for the conservation and sustainable utilization of these plant genetic resources. In this study, we aimed to uncover the genetic landscape of walnuts and potential drivers in the Himalaya for better utilization, awareness, sustainable management and conservation of the extant genetic resources of walnuts in the vast Himalayan landscape.

Location: The Himalaya biodiversity hotspot.

Methods: A total of 1410 wild or feral walnut trees from 65 populations of J. regia and J. sigillata across four countries in the Himalaya were collected. The genetic diversity, population structure, hybridization and gene flow were thoroughly investigated based on the chloroplast genome and 31 nuclear microsatellite markers. The patterns and drivers of the walnut genetic landscape were further explored.

Results: We detected three genetic groups of J. regia (JR1, JR2, JR3), one of J. sigillata (JS) and two hybrid types (JR1 × JS and JR3 × JS) of walnut in the Himalaya, with the western Himalaya identified as the genetic diversity hotspot of J. regia. The spatial genetic pattern of the J. regia was significantly influenced by geographic and climatic factors. Human-mediated dispersal probably promoted the hybridization and gene introgression between J. regia and J. sigillata, which reshaped the genetic landscape of walnut populations in the Himalaya.

Main Conclusions: The extant genetic landscape of walnuts in the Himalaya was driven by natural and anthropogenic forces. Regarding conservation, the western and eastern Himalaya are the genetic reservoir of J. regia and J. sigillata, and hence, pure individuals should be urgently protected from frequent hybridization and introgression. In addition, we propose the utilization of natural hybrid resources coupled with new breeding techniques that combine genomic and phenotypic data.

Original language	English
Article number	e13809
Number of pages	15
Journal	Diversity and Distributions
Volume	30
Issue number	4
Early online date	12 Jan 2024
DOIs	https://doi.org/10.1111/ddi.13809
Publication status	Published - Apr 2024

Keywords / Materials (for Non-textual outputs)

domestication
genetic diversity
Himalaya
hybridization
introgression
walnuts

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10.1111/ddi.13809

Diversity and Distributions - 2024 - Yan - Human‐associated genetic landscape of walnuts in the Himalaya implications forFinal published version, 7.59 MBLicence: Creative Commons: Attribution (CC-BY)

Cite this

Yan, L.-J., Fan, P.-Z., Wambulwa, M. C., Qi, H.-L., Chen, Y., Wu, Z.-Y., Milne, R. I., Khan, R., Luo, Y.-H., Gao, L.-M., Shen, S.-K., Rashid, I., Khan, S. M., Maity, D., Li, D.-Z., & Liu, J. (2024). Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization. Diversity and Distributions, 30(4), Article e13809. https://doi.org/10.1111/ddi.13809

@article{f777c715f6e44dc298923e02eac7a9ac,

title = "Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization",

abstract = "Aims: A comprehensive understanding of the genetic variation of walnuts (Juglans regia and J. sigillata) in the Himalaya and its potential drivers are essential for the conservation and sustainable utilization of these plant genetic resources. In this study, we aimed to uncover the genetic landscape of walnuts and potential drivers in the Himalaya for better utilization, awareness, sustainable management and conservation of the extant genetic resources of walnuts in the vast Himalayan landscape. Location: The Himalaya biodiversity hotspot. Methods: A total of 1410 wild or feral walnut trees from 65 populations of J. regia and J. sigillata across four countries in the Himalaya were collected. The genetic diversity, population structure, hybridization and gene flow were thoroughly investigated based on the chloroplast genome and 31 nuclear microsatellite markers. The patterns and drivers of the walnut genetic landscape were further explored. Results: We detected three genetic groups of J. regia (JR1, JR2, JR3), one of J. sigillata (JS) and two hybrid types (JR1 × JS and JR3 × JS) of walnut in the Himalaya, with the western Himalaya identified as the genetic diversity hotspot of J. regia. The spatial genetic pattern of the J. regia was significantly influenced by geographic and climatic factors. Human-mediated dispersal probably promoted the hybridization and gene introgression between J. regia and J. sigillata, which reshaped the genetic landscape of walnut populations in the Himalaya. Main Conclusions: The extant genetic landscape of walnuts in the Himalaya was driven by natural and anthropogenic forces. Regarding conservation, the western and eastern Himalaya are the genetic reservoir of J. regia and J. sigillata, and hence, pure individuals should be urgently protected from frequent hybridization and introgression. In addition, we propose the utilization of natural hybrid resources coupled with new breeding techniques that combine genomic and phenotypic data.",

keywords = "domestication, genetic diversity, Himalaya, hybridization, introgression, walnuts",

author = "Li-Jun Yan and Peng-Zhen Fan and Wambulwa, {Moses C} and Hai-Ling Qi and Ying Chen and Zeng-Yuan Wu and Milne, {Richard I.} and Raees Khan and Ya-Huang Luo and Lian-Ming Gao and Shi-Kang Shen and Irfan Rashid and Khan, {Shujaul Mulk} and Debabrata Maity and De-Zhu Li and Jie Liu",

note = "Funding Information: We thank Xue‐Wen Liu and Tao Liu for their great help with field sampling. We also thank Lin‐Jiang Ye, Guang‐Fu Zhu, Zhi‐Peng Li, Zuo‐Ying Xiahou, Ikramullah Khan, Ephie A. Magige, Guoquan Wang and other volunteers for their help in the field or laboratory. The authors thank the editors and anonymous reviewers for their insightful suggestions. Molecular experiments were performed at the Laboratory of Molecular Biology at the Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences. This research was funded by the National Natural Science Foundation of China (32170398, 41971071, 42211540718, 31770367, 32160240), the Top‐notch Young Talents Project of Yunnan Provincial {\textquoteleft}Ten Thousand Talents Program{\textquoteright} (YNWR‐QNBJ‐2018‐146), the Xingdian Talent Support Program of Yunnan Province (XDYC‐QNRC‐2022‐0068), CAS {\textquoteleft}Light of West China{\textquoteright} Program, the Natural Science Foundation of Yunnan (202201AT070222), the Key Research Program of Frontier Sciences, CAS (ZDBS‐LY‐7001), and Yunnan Fundamental Research Projects (202201 BC070001). Moses Wambulwa and Raees Khan were supported by the Postdoctoral International Exchange Program of the Office of China Postdoctoral Council, the Postdoctoral Targeted Funding, and Postdoctoral Research Fund of Yunnan Province. Debabrata Maity was supported by Science and Engineering Research Board (CRG/2021/000665) and Ministry of Environment Forest and Climate Change (22018/13/2015‐RE(Tax)), Govt. of lndia, New Delhi. Publisher Copyright: {\textcopyright} 2024 The Authors. Diversity and Distributions published by John Wiley & Sons Ltd.",

year = "2024",

month = apr,

doi = "10.1111/ddi.13809",

language = "English",

volume = "30",

journal = "Diversity and Distributions",

issn = "1366-9516",

publisher = "Wiley-Blackwell",

number = "4",

}

TY - JOUR

T1 - Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization

AU - Yan, Li-Jun

AU - Fan, Peng-Zhen

AU - Wambulwa, Moses C

AU - Qi, Hai-Ling

AU - Chen, Ying

AU - Wu, Zeng-Yuan

AU - Milne, Richard I.

AU - Khan, Raees

AU - Luo, Ya-Huang

AU - Gao, Lian-Ming

AU - Shen, Shi-Kang

AU - Rashid, Irfan

AU - Khan, Shujaul Mulk

AU - Maity, Debabrata

AU - Li, De-Zhu

AU - Liu, Jie

N1 - Funding Information: We thank Xue‐Wen Liu and Tao Liu for their great help with field sampling. We also thank Lin‐Jiang Ye, Guang‐Fu Zhu, Zhi‐Peng Li, Zuo‐Ying Xiahou, Ikramullah Khan, Ephie A. Magige, Guoquan Wang and other volunteers for their help in the field or laboratory. The authors thank the editors and anonymous reviewers for their insightful suggestions. Molecular experiments were performed at the Laboratory of Molecular Biology at the Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences. This research was funded by the National Natural Science Foundation of China (32170398, 41971071, 42211540718, 31770367, 32160240), the Top‐notch Young Talents Project of Yunnan Provincial ‘Ten Thousand Talents Program’ (YNWR‐QNBJ‐2018‐146), the Xingdian Talent Support Program of Yunnan Province (XDYC‐QNRC‐2022‐0068), CAS ‘Light of West China’ Program, the Natural Science Foundation of Yunnan (202201AT070222), the Key Research Program of Frontier Sciences, CAS (ZDBS‐LY‐7001), and Yunnan Fundamental Research Projects (202201 BC070001). Moses Wambulwa and Raees Khan were supported by the Postdoctoral International Exchange Program of the Office of China Postdoctoral Council, the Postdoctoral Targeted Funding, and Postdoctoral Research Fund of Yunnan Province. Debabrata Maity was supported by Science and Engineering Research Board (CRG/2021/000665) and Ministry of Environment Forest and Climate Change (22018/13/2015‐RE(Tax)), Govt. of lndia, New Delhi. Publisher Copyright: © 2024 The Authors. Diversity and Distributions published by John Wiley & Sons Ltd.

PY - 2024/4

Y1 - 2024/4

N2 - Aims: A comprehensive understanding of the genetic variation of walnuts (Juglans regia and J. sigillata) in the Himalaya and its potential drivers are essential for the conservation and sustainable utilization of these plant genetic resources. In this study, we aimed to uncover the genetic landscape of walnuts and potential drivers in the Himalaya for better utilization, awareness, sustainable management and conservation of the extant genetic resources of walnuts in the vast Himalayan landscape. Location: The Himalaya biodiversity hotspot. Methods: A total of 1410 wild or feral walnut trees from 65 populations of J. regia and J. sigillata across four countries in the Himalaya were collected. The genetic diversity, population structure, hybridization and gene flow were thoroughly investigated based on the chloroplast genome and 31 nuclear microsatellite markers. The patterns and drivers of the walnut genetic landscape were further explored. Results: We detected three genetic groups of J. regia (JR1, JR2, JR3), one of J. sigillata (JS) and two hybrid types (JR1 × JS and JR3 × JS) of walnut in the Himalaya, with the western Himalaya identified as the genetic diversity hotspot of J. regia. The spatial genetic pattern of the J. regia was significantly influenced by geographic and climatic factors. Human-mediated dispersal probably promoted the hybridization and gene introgression between J. regia and J. sigillata, which reshaped the genetic landscape of walnut populations in the Himalaya. Main Conclusions: The extant genetic landscape of walnuts in the Himalaya was driven by natural and anthropogenic forces. Regarding conservation, the western and eastern Himalaya are the genetic reservoir of J. regia and J. sigillata, and hence, pure individuals should be urgently protected from frequent hybridization and introgression. In addition, we propose the utilization of natural hybrid resources coupled with new breeding techniques that combine genomic and phenotypic data.

AB - Aims: A comprehensive understanding of the genetic variation of walnuts (Juglans regia and J. sigillata) in the Himalaya and its potential drivers are essential for the conservation and sustainable utilization of these plant genetic resources. In this study, we aimed to uncover the genetic landscape of walnuts and potential drivers in the Himalaya for better utilization, awareness, sustainable management and conservation of the extant genetic resources of walnuts in the vast Himalayan landscape. Location: The Himalaya biodiversity hotspot. Methods: A total of 1410 wild or feral walnut trees from 65 populations of J. regia and J. sigillata across four countries in the Himalaya were collected. The genetic diversity, population structure, hybridization and gene flow were thoroughly investigated based on the chloroplast genome and 31 nuclear microsatellite markers. The patterns and drivers of the walnut genetic landscape were further explored. Results: We detected three genetic groups of J. regia (JR1, JR2, JR3), one of J. sigillata (JS) and two hybrid types (JR1 × JS and JR3 × JS) of walnut in the Himalaya, with the western Himalaya identified as the genetic diversity hotspot of J. regia. The spatial genetic pattern of the J. regia was significantly influenced by geographic and climatic factors. Human-mediated dispersal probably promoted the hybridization and gene introgression between J. regia and J. sigillata, which reshaped the genetic landscape of walnut populations in the Himalaya. Main Conclusions: The extant genetic landscape of walnuts in the Himalaya was driven by natural and anthropogenic forces. Regarding conservation, the western and eastern Himalaya are the genetic reservoir of J. regia and J. sigillata, and hence, pure individuals should be urgently protected from frequent hybridization and introgression. In addition, we propose the utilization of natural hybrid resources coupled with new breeding techniques that combine genomic and phenotypic data.

KW - domestication

KW - genetic diversity

KW - Himalaya

KW - hybridization

KW - introgression

KW - walnuts

U2 - 10.1111/ddi.13809

DO - 10.1111/ddi.13809

M3 - Article

SN - 1366-9516

VL - 30

JO - Diversity and Distributions

JF - Diversity and Distributions

IS - 4

M1 - e13809

ER -

Human-associated genetic landscape of walnuts in the Himalaya: implications for conservation and utilization

Abstract

Keywords / Materials (for Non-textual outputs)

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