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Population genetics informs new insights into the phytogeographic history of Juglans regia L.

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Abstract

Juglans regia is an important perennial crop cultivated for its high-quality nuts and wood. It is generally believed that J. regia survived and expanded in almost completely isolated stands in Asia after the last glaciation. Humans subsequently dispersed J. regia through cultural expansion and trade. We evaluated the spatial genetic structure and genetic diversity of 2,929 J. regia samples from 150 populations using 14 Simple Sequence Repeats (SSRs) markers. Our study revealed that regions with the highest genetic diversity included Southern Asia, Western Asia, Western Europe, and China, as illustrated using a Geostatistical Inverse Distance Weighting (IDW) interpolation of observed heterozygosity (HO), expected (HE) heterozygosity (HE), percentage of polymorphic loci (PPL), the total number of alleles (NA), and Allelic richness (RS) in Arc Geographic Information System (ArcGIS). The ecological Niche Model (ENM) showed J. regia had a high probability of association with Central Asian and Eastern Asian habitats. Population genetic structure, phylogeny, and Principal Coordinate Analysis (PCoA) identified three genetic groups corresponding to three geographic sources. Turkish and Georgian populations served as a bridge between Asian populations and Europe populations. We suggest that J. regia evolved in central Asian mountain ranges ~ 65 million years ago (Mya) and dispersed across Eurasia during climate shifts (~ 65 to 3Mya). The population contracted into multiple refugia during the Last Glacial Maximum. The current distribution of J. regia across Eurasia was shaped by the cumulative effects of contraction or expansion of different refugia and human exploitation after LGM.

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Acknowledgements

The authors extend their appreciation to the Researchers Supporting Project number (RSP-2023R369), King Saud University, Riyadh, Saudi Arabia.

Funding

This work was supported by the National Natural Science Foundation of China (No. 41471038; No. 31200500), the Program for Excellent Young Academic Backbones funding by Northwest University, Shaanxi Academy of Science Research Funding Project (2019 K-06), and Natural Science Foundation of Shaanxi Province of China (2019JM-008). We thank N. Hou, Y. L. Xu, N. Lin, and L. Wang for assisting with sampling. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

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  1. Hanif Khan and Irfan Ullah contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi’an, 710069, Shaanxi, China

    Hanif Khan, Irfan Ullah & Peng Zhao

  2. USDA Forest Service Hardwood Tree Improvement and Regeneration Center (HTIRC), Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, Indiana, 47907, USA

    Keith Woeste

  3. Department of Plant Breeding and Genetics, The University of Haripur, Haripur, 22620, Pakistan

    Sajid Fiaz

  4. Department of Biology, University of Haripur, Haripur, 22620, KP, Pakistan

    Umar Zeb & Azizullah Azizullah

  5. School of Food and Biological Engineering, Jiangsu University Zhenjiang, Zhenjiang, 212013, People’s Republic of China

    Umar Zeb & Fengjie Cui

  6. Department of Plant Production, College of Food and Agriculture Sciences, King Saud University, P.O. Box 2460, Riyadh, 11451, Saudi Arabia

    Abdelhalim I. Ghazy

  7. Department of Chemistry, Faculty of Natural Sciences, The University of Haripur, Haripur, 22620, KPK, Pakistan

    Salma Shad

  8. C.N.R. Institute of Agro-Environmental and Forest Biology, Viale Marconi 2, 05010, Porano, Terni, Italy

    Maria E. Malvolti

  9. Xi’an Botanical Garden of Shaanxi Province, Xi’an, 710061, Shaanxi, People’s Republic of China

    Ming Yue

  10. Department of Biochemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Kotb A. Attia & Arif A. Mohammed

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  1. Hanif Khan
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  2. Irfan Ullah
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Contributions

PZ conceived the idea and conducted research. The investigation was carried out by HK and IU. Data analysis was carried out by HK, KW, ME. M, MY. K A. A, UZ, and SF provided technical expertise. AA, SS, IU, MY, and KW helped in the writing of the original draft. AI. G, A A. M and FC helped in literature improvement, data re-analysis, language modification, funding acquisition and revision of manuscript. All authors carefully read, revise, and approved the article for submission.

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Correspondence to Umar Zeb, Ming Yue or Peng Zhao.

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Experimental research and field studies on plants (either cultivated or wild), including the collection of plant material, complied with relevant institutional, national, and international guidelines and legislation. We also took appropriate permission from the relevant research section of the University during the specimens’ collection and experimentation. We confirm that during the collection and execution of the experiment, the authors have complied with the IUCN Statement on Research Involving Species at Risk of Extinction and the Convention on the Trade in Endangered Species of Wild Fauna and Flora.

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Khan, H., Ullah, I., Woeste, K. et al. Population genetics informs new insights into the phytogeographic history of Juglans regia L.. Genet Resour Crop Evol 70, 2263–2278 (2023). https://doi.org/10.1007/s10722-023-01597-6

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