Tandem gene duplications drive divergent evolution of caffeine and crocin biosynthetic pathways in plants
Zhichao Xu,
Xiangdong Pu,
Ranran Gao,
Olivia Costantina Demurtas,
Steven J. Fleck,
Michaela Richter,
Chunnian He,
Aijia Ji,
Wei Sun,
Jianqiang Kong,
Kaizhi Hu,
Fengming Ren,
Jiejie Song,
Zhe Wang,
Ting Gao,
Chao Xiong,
Haoying Yu,
Tianyi Xin,
Victor A. Albert,
Giovanni Giuliano,
Shilin Chen,
Jingyuan Song
Affiliations
Zhichao Xu
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
Xiangdong Pu
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
Ranran Gao
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
Olivia Costantina Demurtas
Italian National Agency for New Technologies, Energy and Sustainable Economic Development (ENEA), Casaccia Res. Ctr
Steven J. Fleck
Department of Biological Sciences, University at Buffalo
Michaela Richter
Department of Biological Sciences, University at Buffalo
Chunnian He
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
Aijia Ji
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
Wei Sun
Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences
Jianqiang Kong
Institute of Materia Medica, Chinese Academy of Medical Sciences & Peking Union Medical College
Kaizhi Hu
Chongqing Institute of Medicinal Plant Cultivation
Fengming Ren
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
Jiejie Song
College of Life Sciences, Qingdao Agricultural University
Zhe Wang
Institute of Materia Medica, Chinese Academy of Medical Sciences & Peking Union Medical College
Ting Gao
College of Life Sciences, Qingdao Agricultural University
Chao Xiong
Institute of Chinese Materia Medica, China Academy of Chinese Medical Sciences
Haoying Yu
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
Tianyi Xin
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
Victor A. Albert
Department of Biological Sciences, University at Buffalo
Giovanni Giuliano
Italian National Agency for New Technologies, Energy and Sustainable Economic Development (ENEA), Casaccia Res. Ctr
Shilin Chen
Engineering Research Center of Chinese Medicine Resource, Ministry of Education
Jingyuan Song
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
Abstract Background Plants have evolved a panoply of specialized metabolites that increase their environmental fitness. Two examples are caffeine, a purine psychotropic alkaloid, and crocins, a group of glycosylated apocarotenoid pigments. Both classes of compounds are found in a handful of distantly related plant genera (Coffea, Camellia, Paullinia, and Ilex for caffeine; Crocus, Buddleja, and Gardenia for crocins) wherein they presumably evolved through convergent evolution. The closely related Coffea and Gardenia genera belong to the Rubiaceae family and synthesize, respectively, caffeine and crocins in their fruits. Results Here, we report a chromosomal-level genome assembly of Gardenia jasminoides, a crocin-producing species, obtained using Oxford Nanopore sequencing and Hi-C technology. Through genomic and functional assays, we completely deciphered for the first time in any plant the dedicated pathway of crocin biosynthesis. Through comparative analyses with Coffea canephora and other eudicot genomes, we show that Coffea caffeine synthases and the first dedicated gene in the Gardenia crocin pathway, GjCCD4a, evolved through recent tandem gene duplications in the two different genera, respectively. In contrast, genes encoding later steps of the Gardenia crocin pathway, ALDH and UGT, evolved through more ancient gene duplications and were presumably recruited into the crocin biosynthetic pathway only after the evolution of the GjCCD4a gene. Conclusions This study shows duplication-based divergent evolution within the coffee family (Rubiaceae) of two characteristic secondary metabolic pathways, caffeine and crocin biosynthesis, from a common ancestor that possessed neither complete pathway. These findings provide significant insights on the role of tandem duplications in the evolution of plant specialized metabolism.
