Haplotype-resolved genome reveals allele-aware epigenetic and 3D chromatin regulation of heterosis in the tea hybrid.

Journal: The New phytologist
Published Date:

Abstract

Heterosis, widely used in plant breeding to enhance yield and quality, is not yet fully understood at the allelic level, particularly in woody plants such as Camellia sinensis, the tea plant. In this study, the first haplotype (HA)-resolved genome of JGY, the most widely cultivated hybrid oolong tea cultivar in China, is presented, and the contribution of its epigenetic and 3D genomic features to heterosis is explored. It was revealed that CHG methylation in gene bodies serves as a key epigenetic predictor of allele-specific expression (ASE), as identified by machine learning models. Additionally, it was shown that allele-specific chromatin accessibility plays a significant role in regulating ASE, with specific chromatin regions in the promoter of CsDXS2, a key enzyme in the methylerythritol phosphate (MEP) terpene biosynthesis pathway, being responsible for the modulation of its expression through CsBZIP48. Furthermore, HA-resolved Hi-C analysis uncovered large-scale chromatin reorganization in the hybrid, including A/B compartment switching and topologically associating domain (TAD) reorganization, which are linked to changes in gene expression, particularly in aroma-related genes. These findings highlight the coordinated reprogramming of parental epigenetic and 3D genomic features during hybridization and provide new insights into the molecular mechanisms underlying heterosis in woody plants.

Authors

  • Wenlong Lei
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Yingao Zhang
    Gynecologic Oncology Division, Department of Obstetrics and Gynecology, University of North Carolina School of Medicine (Drs. Zhang, Paraghamian, Clark, and Ms. Grant). Electronic address: [email protected].
  • Yibin Wang
    Department of Engineering, Sichuan Normal University, Chengdu, Sichuan, 610066, China.
  • Jiaxin Yu
    AI Innovation Center, China Medical University Hospital, Taichung, Taiwan. [email protected].
  • Huike Li
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Xinru Hou
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Wenmin Fan
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Yezi Xiao
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Jiawei Yan
    Department of Chemistry, Stanford University, Stanford, California 94305, USA.
  • Xiaomei Lei
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Shuai Chen
    State Key Laboratory of Resources and Environmental Information Systems, Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, China.
  • Weidong Wang
    Zhejiang Huade New Materials Co., Ltd., Zhejiang Province, Hangzhou, China.
  • Qingshan Xu
    School of Civil Aviation, Northwestern Polytechnical University, Xi'an 710072, China.
  • Naixing Ye
    College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.
  • Youben Yu
    College of Horticulture, Northwest A&F University, Yangling, 712100, China.
  • Xingtan Zhang
    National Key Laboratory for Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, Guangzhou 518120, China.
  • Pengjie Wang
    Department of Nutrition and Health, China Agricultural University, Beijing 100193, China.

Keywords

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