Crocus genome reveals the evolutionary origin of crocin biosynthesis

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 re...

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Main Authors: 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
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:Acta Pharmaceutica Sinica B
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S221138352300494X
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author 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
author_facet 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
author_sort Zhichao Xu
collection DOAJ
description 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.
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spelling doaj.art-a7aaa9dcbcc340039c65371440638b872024-03-23T06:24:04ZengElsevierActa Pharmaceutica Sinica B2211-38352024-04-0114418781891Crocus genome reveals the evolutionary origin of crocin biosynthesisZhichao Xu0Shanshan Chen1Yalin Wang2Ya Tian3Xiaotong Wang4Tianyi Xin5Zishan Li6Xin Hua7Shengnan Tan8Wei Sun9Xiangdong Pu10Hui Yao11Ranran Gao12Jingyuan Song13Key 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; 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; College of Life Science, Northeast Forestry University, Harbin 150040, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, China; 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, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, China; 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, ChinaKey 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; 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, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, ChinaCollege of Life Science, Northeast Forestry University, Harbin 150040, ChinaAnalysis and Testing Center of Northeast Forestry University, Harbin 150040, ChinaKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, China Academy of Chinese Medical Sciences, Institute of Chinese Materia Medica, Beijing 100700, ChinaSchool of Pharmacy, Anhui Medical University, Inflammation and Immune Mediated Diseases Laboratory of Anhui Province, Hefei 230032, ChinaKey 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; 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, ChinaKey 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; Corresponding authors.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; 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; Corresponding authors.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.http://www.sciencedirect.com/science/article/pii/S221138352300494XCrocus sativusWGTCrocin biosynthesisCarotenoidsApocarotenoidsCCDs
spellingShingle 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
Crocus genome reveals the evolutionary origin of crocin biosynthesis
Acta Pharmaceutica Sinica B
Crocus sativus
WGT
Crocin biosynthesis
Carotenoids
Apocarotenoids
CCDs
title Crocus genome reveals the evolutionary origin of crocin biosynthesis
title_full Crocus genome reveals the evolutionary origin of crocin biosynthesis
title_fullStr Crocus genome reveals the evolutionary origin of crocin biosynthesis
title_full_unstemmed Crocus genome reveals the evolutionary origin of crocin biosynthesis
title_short Crocus genome reveals the evolutionary origin of crocin biosynthesis
title_sort crocus genome reveals the evolutionary origin of crocin biosynthesis
topic Crocus sativus
WGT
Crocin biosynthesis
Carotenoids
Apocarotenoids
CCDs
url http://www.sciencedirect.com/science/article/pii/S221138352300494X
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