Crocus genome reveals the evolutionary origin of crocin biosynthesis

Zhichao Xu; Shanshan Chen; Yalin Wang; Ya Tian; Xiaotong Wang; Tianyi Xin; Zishan Li; Xin Hua; Shengnan Tan; Wei Sun; Xiangdong Pu; Hui Yao; Ranran Gao; Jingyuan Song

doi:10.1016/j.apsb.2023.12.013

Crocus genome reveals the evolutionary origin of crocin biosynthesis

Acta Pharm Sin B. 2024 Apr;14(4):1878-1891. doi: 10.1016/j.apsb.2023.12.013. Epub 2023 Dec 27.

Authors

Zhichao Xu^{1

2

3}, Shanshan Chen^{3

4}, Yalin Wang³, Ya Tian³, Xiaotong Wang^{3

4}, Tianyi Xin^{1

2}, Zishan Li³, Xin Hua³, Shengnan Tan⁵, Wei Sun⁴, Xiangdong Pu⁶, Hui Yao^{1

2}, Ranran Gao⁴, Jingyuan Song^{1

2}

Affiliations

¹ Key Lab of Chinese Medicine Resources Conservation, State Administration of Traditional Chinese Medicine of the People's Republic of China, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing 100193, China.
² State Key Laboratory of Basis and New Drug Development of Natural and Nuclear Drugs, Engineering Research Center of Chinese Medicine Resource, Ministry of Education, Beijing 100193, China.
³ College of Life Science, Northeast Forestry University, Harbin 150040, China.
⁴ Key Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, China Academy of Chinese Medical Sciences, Institute of Chinese Materia Medica, Beijing 100700, China.
⁵ Analysis and Testing Center of Northeast Forestry University, Harbin 150040, China.
⁶ School of Pharmacy, Anhui Medical University, Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, Hefei 230032, China.

Abstract

Crocus sativus (saffron) is a globally autumn-flowering plant, and its stigmas are the most expensive spice and valuable herb medicine. Crocus specialized metabolites, crocins, are biosynthesized in distant species, Gardenia (eudicot) and Crocus (monocot), and the evolution of crocin biosynthesis remains poorly understood. With the chromosome-level Crocus genome assembly, we revealed that two rounds of lineage-specific whole genome triplication occurred, contributing important roles in the production of carotenoids and apocarotenoids. According to the kingdom-wide identification, phylogenetic analysis, and functional assays of carotenoid cleavage dioxygenases (CCDs), we deduced that the duplication, site positive selection, and neofunctionalization of Crocus-specific CCD2 from CCD1 members are responsible for the crocin biosynthesis. In addition, site mutation of CsCCD2 revealed the key amino acids, including I143, L146, R161, E181, T259, and S292 related to the catalytic activity of zeaxanthin cleavage. Our study provides important insights into the origin and evolution of plant specialized metabolites, which are derived by duplication events of biosynthetic genes.

Keywords: Apocarotenoids; CCDs; Carotenoids; Crocin biosynthesis; Crocus sativus; WGT.

Associated data

figshare/10.6084/m9.figshare.21988667