Selective and comparative genome architecture of Asian cultivated rice (Oryza sativa L.) attributed to domestication and modern breeding

Xueqiang Wang; Wensheng Wang; Shuaishuai Tai; Min Li; Qiang Gao; Zhiqiang Hu; Wushu Hu; Zhichao Wu; Xiaoyang Zhu; Jianyin Xie; Fengmei Li; Zhifang Zhang; Linran Zhi; Fan Zhang; Xiaoqian Ma; Ming Yang; Jiabao Xu; Yanhong Li; Wenzhuo Zhang; Xiyu Yang; Ying Chen; Yan Zhao; Binying Fu; Xiuqin Zhao; Jinjie Li; Miao Wang; Zhen Yue; Xiaodong Fang; Wei Zeng; Ye Yin; Gengyun Zhang; Jianlong Xu; Hongliang Zhang; Zichao Li; Zhikang Li

doi:10.1016/j.jare.2022.08.004

Selective and comparative genome architecture of Asian cultivated rice (Oryza sativa L.) attributed to domestication and modern breeding

J Adv Res. 2022 Dec:42:1-16. doi: 10.1016/j.jare.2022.08.004. Epub 2022 Aug 18.

Authors

Xueqiang Wang¹, Wensheng Wang², Shuaishuai Tai³, Min Li⁴, Qiang Gao³, Zhiqiang Hu⁵, Wushu Hu³, Zhichao Wu⁵, Xiaoyang Zhu⁶, Jianyin Xie⁶, Fengmei Li⁶, Zhifang Zhang⁶, Linran Zhi⁶, Fan Zhang², Xiaoqian Ma⁶, Ming Yang³, Jiabao Xu³, Yanhong Li³, Wenzhuo Zhang⁶, Xiyu Yang⁶, Ying Chen⁷, Yan Zhao⁶, Binying Fu⁵, Xiuqin Zhao⁵, Jinjie Li⁶, Miao Wang³, Zhen Yue³, Xiaodong Fang³, Wei Zeng⁴, Ye Yin³, Gengyun Zhang⁸, Jianlong Xu⁹, Hongliang Zhang¹⁰, Zichao Li¹¹, Zhikang Li¹²

Affiliations

¹ State Key Laboratory of Agrobiotechnology / Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China; Institute of Crop Science, Plant Precision Breeding Academy, Zhejiang Provincial Key Laboratory of Crop Genetic Resources, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China.
² Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; The College of Agronomy, Anhui Agricultural University, Hefei, China.
³ BGI Genomics, BGI-Shenzhen, Shenzhen 518083, China.
⁴ The College of Agronomy, Anhui Agricultural University, Hefei, China.
⁵ Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
⁶ State Key Laboratory of Agrobiotechnology / Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China.
⁷ College of Information and Electrical Engineering, China Agricultural University, Beijing 100193, China.
⁸ BGI Genomics, BGI-Shenzhen, Shenzhen 518083, China; State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, Shenzhen 518083, China.
⁹ Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; 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, China.
¹⁰ State Key Laboratory of Agrobiotechnology / Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China. Electronic address: zhangl@cau.edu.cn.
¹¹ State Key Laboratory of Agrobiotechnology / Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China. Electronic address: lizichao@cau.edu.cn.
¹² Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; The College of Agronomy, Anhui Agricultural University, Hefei, China; 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, China. Electronic address: lizhikang@caas.cn.

Abstract

Introduction: Rice, Oryza sativa L. (Os), is one of the oldest domesticated cereals that has also gone through extensive improvement in modern breeding.

Objectives: How rice was domesticated and impacted by modern breeding.

Methods: We performed comprehensive analyses of genomic sequences of 504 accessions of Os and 456 accessions of O. rufipogon/O. nivara (Or).

Results: The natural selection on Or before domestication and the natural and artificial selection during domestication together shaped the well-differentiated genomes of two subspecies, geng(j) (japonica) and xian(i) (indica), while breeding has made apparent genomic imprints between landrace and modern varieties of each subspecies, and also between primary modern and advanced modern varieties of xian(i). Selection during domestication and breeding left genome-wide selective signals covering ∼ 22.8 % and ∼ 8.6 % of the Os genome, significantly reduced within-population genomic diversity by ∼ 22 % in xian(i) and ∼ 53 % in geng(j) plus more pronounced subspecific differentiation. Only ∼ 10 % reduction in the total genomic diversity was observed between the Os and Or populations, indicating domestication did not suffer severe genetic bottleneck.

Conclusion: Our results revealed clear differentiation of the Or accessions into three large populations, two of which correspond to the well-differentiated Os subspecies, geng(j) and xian(i). Improved productivity and common changes in the same suit of adaptive traits in xian(i) and geng(j) during domestication and breeding resulted apparently from compensatory and convergent selections for different genes/alleles acting in the common KEGG terms and/or same gene families, and thus maintaining or even increasing the within population diversity and subspecific differentiation of Os, while more genes/alleles of novel function were selected during domestication than modern breeding. Our results supported the multiple independent domestication of Os in Asia and suggest the more efficient utilization of the rich diversity within Os by exploiting inter-subspecific and among population diversity in future rice improvement.

Keywords: Domestication; Modern breeding; Novel functional variation selection; Oryza sativa; Standing functional variation selection.

Publication types

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

MeSH terms

Crops, Agricultural / genetics
Domestication
Genomics
Oryza* / genetics
Plant Breeding