Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication

First author: Dan Zhang; Affiliations: Henan Agricultural University (河南农业大学): Zhengzhou, China

Corresponding author: Dan Zhang

Increasing seed oil content is one of the most important breeding goals for soybean due to a high global demand for edible vegetable oil. However, genetic improvement of seed oil content has been difficult in soybean because of the complexity of oil metabolism. Determining the major variants and molecular mechanisms conferring oil accumulation is critical for substantial oil enhancement in soybean and other oilseed crops. In this study, we evaluated the seed oil contents of 219 diverse soybean accessions across six different environments and dissected the underlying mechanism using a high-resolution genome-wide association study (GWAS). An environmentally stable quantitative trait locus (QTL), GqOil20, significantly associated with oil content was identified, accounting for 23.70% of the total phenotypic variance of seed oil across multiple environments. Haplotype and expression analyses indicate that an oleosin protein-encoding gene (GmOLEO1), colocated with a leading single nucleotide polymorphism (SNP) from the GWAS, was significantly correlated with seed oil content. GmOLEO1 is predominantly expressed during seed maturation, and GmOLEO1 is localized to accumulated oil bodies (OBs) in maturing seeds. Overexpression of GmOLEO1 significantly enriched smaller OBs and increased seed oil content by 10.6% compared with those of control seeds. A time-course transcriptomics analysis between transgenic and control soybeans indicated that GmOLEO1 positively enhanced oil accumulation by affecting triacylglycerol metabolism. Our results also showed that strong artificial selection had occurred in the promoter region of GmOLEO1, which resulted in its high expression in cultivated soybean relative to wild soybean, leading to increased seed oil accumulation. The GmOLEO1 locus may serve as a direct target for both genetic engineering and selection for soybean oil improvement.

由于全球对食用植物油的高需求，增加种子油含量是大豆育种最主要的目标之一。然而，由于大豆油类代谢的复杂性，对于其种子油含量的遗传改良一直十分困难。鉴定大豆中影响油积累的主要变异因素及潜在分子机理对于大豆和其它油料作物的油增产至关重要。本文中，作者研究了来自6个不同生长环境的219份大豆材料的种子油含量，并通过一个高分辨率的全基因组关联分析解析了大豆种子油含量的潜在遗传基础。作者鉴定到了一个不同环境下稳定的数量性状位点GqOil20显著与种子油含量相关，并且贡献了不同环境下油含量表型变异的23.7%。单倍型和表达分析显示一个油体蛋白编码基因GmOLEO1与一个从GWAS中鉴定的一个主要单核苷酸变异位点共定位，并显著与种子油含量相关。GmOLEO1基因主要在种子成熟过程中表达，并且GmOLEO1蛋白在成熟种子中定位于积累的油体中。一个转基因和对照的时间序列转录组分析显示GmOLEO1基因可以通过影响甘油三酯的代谢来增加种子的油含量。作者的研究同时还显示GmOLEO1基因的启动子区存在强烈的人工选择信号，从而导致其在栽培种大豆中的表达远高于野生种，最终使得栽培种大豆的种子产油量增加。GmOLEO1位点可以作为大豆油改良中遗传工程和选择的直接靶位点。

通讯：张丹 (http://nongxue.henau.edu.cn/a/jiaoshifengcai/zwyz/20161212/3966.html)

个人简介：2001-2005年，河南农业大学，学士；2005-2010年，南京农业大学，硕、博士。

研究方向：大豆品质与抗逆重要基因的发掘与分子机制研究。

doi: https://doi.org/10.1371/journal.pgen.1008267

Journal: PLOS Genetics

Published date: July 10, 2019