The Chinese pine genome and methylome unveil key features of conifer evolution

Shihui Niu; Jiang Li; Wenhao Bo; Weifei Yang; Andrea Zuccolo; Stefania Giacomello; Xi Chen; Fangxu Han; Junhe Yang; Yitong Song; Yumeng Nie; Biao Zhou; Peiyi Wang; Quan Zuo; Hui Zhang; Jingjing Ma; Jun Wang; Lvji Wang; Qianya Zhu; Huanhuan Zhao; Zhanmin Liu; Xuemei Zhang; Tao Liu; Surui Pei; Zhimin Li; Yao Hu; Yehui Yang; Wenzhao Li; Yanjun Zan; Linghua Zhou; Jinxing Lin; Tongqi Yuan; Wei Li; Yue Li; Hairong Wei; Harry X Wu

doi:10.1016/j.cell.2021.12.006

The Chinese pine genome and methylome unveil key features of conifer evolution

Cell. 2022 Jan 6;185(1):204-217.e14. doi: 10.1016/j.cell.2021.12.006. Epub 2021 Dec 28.

Authors

Shihui Niu¹, Jiang Li², Wenhao Bo², Weifei Yang³, Andrea Zuccolo⁴, Stefania Giacomello⁵, Xi Chen², Fangxu Han², Junhe Yang², Yitong Song², Yumeng Nie², Biao Zhou², Peiyi Wang², Quan Zuo², Hui Zhang², Jingjing Ma², Jun Wang², Lvji Wang², Qianya Zhu², Huanhuan Zhao², Zhanmin Liu⁶, Xuemei Zhang³, Tao Liu³, Surui Pei³, Zhimin Li³, Yao Hu⁷, Yehui Yang⁷, Wenzhao Li⁷, Yanjun Zan⁸, Linghua Zhou⁸, Jinxing Lin², Tongqi Yuan⁹, Wei Li², Yue Li², Hairong Wei¹⁰, Harry X Wu¹¹

Affiliations

¹ Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, P.R. China. Electronic address: arrennew@bjfu.edu.cn.
² Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, P.R. China.
³ Annoroad Gene Technology (Beijing) Co., Ltd, Beijing 100180, P.R. China.
⁴ Center for Desert Agriculture, Biological and Environmental Sciences & Engineering Division (BESE), King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia; Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy.
⁵ SciLife Lab, KTH Royal Institute of Technology, Tomtebodavägen 23, SE-171 65 Stockholm, Sweden.
⁶ Qigou State-owned Forest Farm, Pingquan, Hebei Province 067509, P. R. China.
⁷ Alibaba Group, Hangzhou 311121, P.R. China.
⁸ Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Linnaeus väg 6, 901 83 Umeå, Sweden.
⁹ Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, P.R. China; College of Material Science and Technology, Beijing Forestry University, Beijing 100083, P.R. China.
¹⁰ College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI 49931, USA. Electronic address: hairong@mtu.edu.
¹¹ Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, The Tree and Ornamental Plant Breeding and Biotechnology Laboratory of National Forestry and Grassland Administration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, P.R. China; Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Linnaeus väg 6, 901 83 Umeå, Sweden; CSIRO National Research Collection Australia, Black Mountain Laboratory, Canberra, ACT 2601, Australia. Electronic address: harry.wu@slu.se.

PMID: 34965378
DOI: 10.1016/j.cell.2021.12.006

Abstract

Conifers dominate the world's forest ecosystems and are the most widely planted tree species. Their giant and complex genomes present great challenges for assembling a complete reference genome for evolutionary and genomic studies. We present a 25.4-Gb chromosome-level assembly of Chinese pine (Pinus tabuliformis) and revealed that its genome size is mostly attributable to huge intergenic regions and long introns with high transposable element (TE) content. Large genes with long introns exhibited higher expressions levels. Despite a lack of recent whole-genome duplication, 91.2% of genes were duplicated through dispersed duplication, and expanded gene families are mainly related to stress responses, which may underpin conifers' adaptation, particularly in cold and/or arid conditions. The reproductive regulation network is distinct compared with angiosperms. Slow removal of TEs with high-level methylation may have contributed to genomic expansion. This study provides insights into conifer evolution and resources for advancing research on conifer adaptation and development.

Keywords: Chinese pine; chromosome-level genome; climate adaptation; conifer evolution; conifer reproduction; gene expression; genome expansion; long intron; methylome.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Acclimatization / genetics
Chromosomes, Plant / genetics
Cycadopsida / genetics
DNA Transposable Elements / genetics
Epigenome*
Evolution, Molecular*
Forests
Gene Expression Regulation, Plant*
Gene Regulatory Networks
Genes, Plant*
Genome Size
Genomics / methods
Introns
Magnoliopsida / genetics
Pinus / genetics*

Substances

DNA Transposable Elements