Tandem gene duplications drive divergent evolution of caffeine and crocin biosynthetic pathways in plants
Year: 2020
Type: article
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.
Source: BMC Biology
Authors: 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, Jiejie Song, Zhe Wang, Ting Gao, Chao Xiong, Haoying Yu, Tianyi Xin, Victor A. Albert, Giovanni Giuliano, Shilin Chen, Jingyuan Song, Jingyuan Song
Institutions: Ministry of Education of the People's Republic of China, Chinese Academy of Medical Sciences & Peking Union Medical College, State Administration of Traditional Chinese Medicine of the People's Republic of China, Institute of Medicinal Plant Development, National Agency for New Technologies, Energy and Sustainable Economic Development, University at Buffalo, State University of New York, China Academy of Chinese Medical Sciences, Institute of Chinese Materia Medica, Qingdao Agricultural University, Nanyang Technological University, ENEA Casaccia Research Centre
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: gold
Estimated APC paid: $2,990
Awards: G1451932349, From DISCOvery to products: A next generation pipeline for the sustainable generation of high-value plant products, Dimensions: Collaborative Proposal: Molecular, ecological and evolutionary dynamics of carbon fixation and diversification in Agavoideae (Asparagaceae) and Oncidiinae (Orchidaceae), G846127912, G864074006
OpenAlex ID: W3036938386