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

Authors: ZHANG, DAN - Henan Agricultural University; ZHANG, HENGYOU - University Of North Carolina; HU, ZHENBIN - Kansas State University; CHU, SHANSHAN - Nanjing Agricultural University; YU, KAIYE - Nanjing Agricultural University; LV, LINGLING - Nanjing Agricultural University; YANG, YUMING - Nanjing Agricultural University; ZHANG, XIANGQIANG - Nanjing Agricultural University; CHEN, XI - Nanjing Agricultural University; KAN, GUIZHEN - Nanjing Agricultural University; TANG, YANG - Nanjing Agricultural University; An, Yong-Qiang - Charles; YU, DEYUE - Nanjing Agricultural University

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/22/2019
Publication Date: 7/10/2019
Citation: Zhang, D., Zhang, H., Hu, Z., Chu, S., Yu, K., Lv, L., Yang, Y., Zhang, X., Chen, X., Kan, G., Tang, Y., An, Y., Yu, D. 2019. Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication. PLoS Genetics. 15(7):e1008267. https://doi.org/10.1371/journal.pgen.1008267.
DOI: https://doi.org/10.1371/journal.pgen.1008267

Interpretive Summary: The high value of seed oil is one of the major driving factors for worldwide demand for soybean. Developing soybean cultivars with improved oil content will increase U.S. soybean competitiveness worldwide, as well as U.S. soybean growers’ income. However, effective soybean genetic improvement for higher oil content is hindered by lack of availability of genes/gene variants controlling oil accumulation and understanding of their underlying molecular mechanism. Having applied inter-disciplinary approaches, we identified a soybean gene underlying an environmentally-stable genetic locus that accounted for 24% of seed oil variation. Over-expression of the gene in soybean increased seed oil content by 11% without yield penalty. We also investigated its underlying molecular and cellular mechanism. The gene can serve as a target for soybean oil improvement through both genetic engineering and molecular breeding.

Technical Abstract: Effective soybean genetic improvement for higher oil content is hindered by lack of availability of genes/gene variants controlling oil accumulation and understanding of their underlying molecular mechanism. We evaluated the seed oil content in 219 diverse soybean accessions across six different environments and identified a major environmentally-stable QTL using high-density genome wide association study. The QTL accounted for 23.70% of seed oil variance across multi-environments. Haplotype and expression analyses indicate that a membrane-associated oleosin protein-encoding gene (GmOLEO1) significantly correlated with seed oil content. GmOLEO1 are specifically expressed during seed maturation and its products localized on oil bodies (OBs) in maturing seeds. Over-expression of GmOLEO1 significantly enriched smaller OBs and increased seed oil content by 10.6% without yield penalty. A time-course transcriptomic analyses between transgenic and control soybeans indicated that GmOLEO1 positively affecting oil accumulation through enhancing triacylglycerol metabolism. Our results also showed that a strong artificial selection occurred in the promoter region of GmOLEO1, leading its higher expression in cultivated soybean relative to wild soybean. Our results indicated that GmOLEO1 showed conserved roles in enriching smaller OBs during seed maturation in plants while possessed novel characteristics in enhancing oil accumulation in soybean seeds. It might serve as a direct target for soybean oil improvement through gene engineering or molecular breeding.