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The complex genome and adaptive evolution of polyploid Chinese pepper (Zanthoxylum armatum and Zanthoxylum bungeanum)
Authors:Lisong Hu  Zhongping Xu  Rui Fan  Guanying Wang  Fuqiu Wang  Xiaowei Qin  Lin Yan  Xunzhi Ji  Minghui Meng  Soonliang Sim  Wei Chen  Chaoyun Hao  Qinghuang Wang  Huaguo Zhu  Shu Zhu  Pan Xu  Hui Zhao  Keith Lindsey  Henry Daniell  Jonathan F. Wendel  Shuangxia Jin
Affiliation:1. Spice and Beverage Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wanning, China

Ministry of Agriculture Key Laboratory of Genetic Resources Utilization of Spice and Beverage Crops, Wanning, China

Key Laboratory of Genetic Improvement and Quality Regulation for Tropical Spice and Beverage Crops of Hainan Province, Wanning, China

These authors contributed equally.;2. Spice and Beverage Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wanning, China;3. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China;4. Spice and Beverage Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wanning, China

Ministry of Agriculture Key Laboratory of Genetic Resources Utilization of Spice and Beverage Crops, Wanning, China

Key Laboratory of Genetic Improvement and Quality Regulation for Tropical Spice and Beverage Crops of Hainan Province, Wanning, China;5. State Key Laboratory of Grassland and Agro-Ecosystems, School of Life Sciences, Lanzhou University, Lanzhou, China;6. Academy of Sciences Malaysia, Kuala Lumpur, Malaysia;7. College of Biology and Agricultural Resources, Huanggang Normal University, Huanggang, Hubei, China;8. Jinjiaohong Spice Research Institute, Jinjiaohong Agricultural Technology Group Corporation, Nanjing, China;9. Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Haikou, China;10. Department of Biosciences, Durham University, Durham, UK;11. Department of Biochemistry, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA;12. Department Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA

Abstract:Zanthoxylum armatum and Zanthoxylum bungeanum, known as ‘Chinese pepper’, are distinguished by their extraordinary complex genomes, phenotypic innovation of adaptive evolution and species-special metabolites. Here, we report reference-grade genomes of Z. armatum and Z. bungeanum. Using high coverage sequence data and comprehensive assembly strategies, we derived 66 pseudochromosomes comprising 33 homologous phased groups of two subgenomes, including autotetraploid Z. armatum. The genomic rearrangements and two whole-genome duplications created large (~4.5 Gb) complex genomes with a high ratio of repetitive sequences (>82%) and high chromosome number (2n = 4x = 132). Further analysis of the high-quality genomes shed lights on the genomic basis of involutional reproduction, allomones biosynthesis and adaptive evolution in Chinese pepper, revealing a high consistent relationship between genomic evolution, environmental factors and phenotypic innovation. Our study provides genomic resources and new insights for investigating diversification and phenotypic innovation in Chinese pepper, with broader implications for the protection of plants under severe environmental changes.
Keywords:Chinese pepper (Zanthoxylum armatum and Zanthoxylum bungeanum)  polyploid  identified subgenomes  phenotypic innovation  adaptive evolution
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