Whole-genome resequencing of Osmanthus fragrans provides insights into flower color evolution

Hongguo Chen,Siwei Xiao,Xinxin Yi,Jie Yang,Xiangling Zeng,Zhenqi Wang,Jingjing Zou,Qiang Fu,Junyi Liu,Riru Zheng,Xuan Cai,Caiyun Wang,Yumin Shi

doi:10.1038/s41438-021-00531-0

Abstract

Osmanthus fragrans is a well-known ornamental plant that has been domesticated in China for 2500 years. More than 160 cultivars have been found during this long period of domestication, and they have subsequently been divided into four cultivar groups, including the Yingui, Jingui, Dangui, and Sijigui groups. These groups provide a set of materials to study genetic evolution and variability. Here, we constructed a reference genome of O. fragrans ‘Liuyejingui’ in the Jingui group and investigated its floral color traits and domestication history by resequencing a total of 122 samples, including 119 O. fragrans accessions and three other Osmanthus species, at an average sequencing depth of 15×. The population structure analysis showed that these 119 accessions formed an apparent regional cluster. The results of linkage disequilibrium (LD) decay analysis suggested that varieties with orange/red flower color in the Dangui group had undergone more artificial directional selection; these varieties had the highest LD values among the four groups, followed by the Sijigui, Jingui, and Yingui groups. Through a genome-wide association study, we further identified significant quantitative trait loci and genomic regions containing several genes, such as ethylene-responsive transcription factor 2 and Arabidopsis pseudoresponse regulator 2, that are positively associated with petal color. Moreover, we found a frameshift mutation with a 34-bp deletion in the first coding region of the carotenoid cleavage dioxygenase 4 gene. This frameshift mutation existed in at least one site on both alleles in all varieties of the Dangui group. The results from this study shed light on the genetic basis of domestication in woody plants, such as O. fragrans.

Highlights

Sweet osmanthus (Osmanthus fragrans Lour.), belonging to the family Oleaceae, is a well-known ornamental germplasm native to the Sino-Himalayan region[1]
These Aa genotype samples in other groups were clustered closely to the ‘Dangui group’ on the phylogenetic tree (Fig. 3a). These results showed that the frameshift mutation of the CCD4 gene is probably related to the formation of orange/red flower color in O. fragrans
In this study, we successfully sequenced and assembled a reference genome for O. fragrans ‘Liuyejingui’ (OFL), an autumn-flowering cultivar harvested for its economic value, by combining results from the Illumina, PacBio and highthroughput chromatin conformation capture (Hi-C) platforms

Summary

Introduction

Sweet osmanthus (Osmanthus fragrans Lour.), belonging to the family Oleaceae, is a well-known ornamental germplasm native to the Sino-Himalayan region[1]. The evolutionary relationships of varieties with different colors are still not clear Due to their ornamental and commercial value, flowers have long been a focus of interest in the study of O. fragrans. The main differences in flower color and floral fragrance among varieties in different groups of O. fragrans are determined mainly by the degree of carotenoid accumulation and cleavage. The most critical factor determining the diversity of carotenoid concentrations was the differential expression level of CCD410,12 This leads to the question, what role does the CCD4 gene play in the evolution of O. fragrans flower color?

Results

Discussion

Conclusion