The Tetracentron genome provides insight into the early evolution of eudicots and the formation of vessel elements

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The Tetracentron genome provides insight into the early evolution of eudicots and the formation of vessel elements Ping-Li Liu1,2†, Xi Zhang1,2†, Jian-Feng Mao1,2†, Yan-Ming Hong1,2†, Ren-Gang Zhang3, Yilan E1,2, Shuai Nie1,2, Kaihua Jia1,2, Chen-Kun Jiang4, Jian He5, Weiwei Shen1,2, Qizouhong He1,2, Wenqing Zheng1,2, Samar Abbas1,2, Pawan Kumar Jewaria1,2, Xuechan Tian1,2, Chang-jun Liu6, Xiaomei Jiang7,8, Yafang Yin7,8, Bo Liu7,8, Li Wang9, Biao Jin9, Yongpeng Ma10, Zongbo Qiu11, František Baluška12, Jozef Šamaj13, Xinqiang He14, Shihui Niu1,2, Jianbo Xie1,2, Lei Xie5, Huimin Xu15, Hongzhi Kong16, Song Ge16, Richard A. Dixon1,17, Yuannian Jiao16* and Jinxing Lin1,2* * Correspondence: [email protected]. cn; [email protected] † Ping-Li Liu, Xi Zhang, Jian-Feng Mao and Yan-Ming Hong contributed equally to this work. 16 Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China 1 Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, China Full list of author information is available at the end of the article

Abstract Background: Tetracentron sinense is an endemic and endangered deciduous tree. It belongs to the Trochodendrales, one of four early diverging lineages of eudicots known for having vesselless secondary wood. Sequencing and resequencing of the T. sinense genome will help us understand eudicot evolution, the genetic basis of tracheary element development, and the genetic diversity of this relict species. Results: Here, we report a chromosome-scale assembly of the T. sinense genome. We assemble the 1.07 Gb genome sequence into 24 chromosomes and annotate 32, 690 protein-coding genes. Phylogenomic analyses verify that the Trochodendrales and core eudicots are sister lineages and showed that two whole-genome duplications occurred in the Trochodendrales approximately 82 and 59 million years ago. Synteny analyses suggest that the γ event, resulting in paleohexaploidy, may have only happened in core eudicots. Interestingly, we find that vessel elements are present in T. sinense, which has two orthologs of AtVND7, the master regulator of vessel formation. T. sinense also has several key genes regulated by or regulating TsVND7.2 and their regulatory relationship resembles that in Arabidopsis thaliana. Resequencing and population genomics reveals high levels of genetic diversity of T. sinense and identifies four refugia in China. Conclusions: The T. sinense genome provides a unique reference for inferring the early evolution of eudicots and the mechanisms underlying vessel element formation. Population genomics analysis of T. sinense reveals its genetic diversity and geographic structure with implications for conservation. Keywords: Tetracentron sinense, Vessel, Phylogenomic, Whole genome duplication, VND7, Resequencing, Genetic diversity

© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and re