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Tandem gene duplications drive divergent evolution of caffeine and crocin biosynthetic pathways in plants

TitoloTandem gene duplications drive divergent evolution of caffeine and crocin biosynthetic pathways in plants
Tipo di pubblicazioneArticolo su Rivista peer-reviewed
Anno di Pubblicazione2020
AutoriXu, Z., Xu Z., Pu X., Gao R., Demurtas Olivia Costantina, Fleck S.J., Richter M., He C., He C., Ji A., Sun W., Kong J., Hu K., Ren F., Ren F., Song J., Wang Z., Gao T., Xiong C., Yu H., Xin T., Albert V.A., Albert V.A., Giuliano Giovanni, Chen S., Chen S., Song J., Song J., and Song J.
RivistaBMC Biology
Volume18
Paginazione1–14
ISSN17417007
Parole chiavebiosynthesis, Biosynthetic Pathways, Caffeine, Carotenoid, Carotenoids, crocin, Evolution, Gardenia, Gene duplication, genetics, Genome, metabolism, Molecular, molecular evolution, Plant, plant genome
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. © 2020 The Author(s).

Note

cited By 37

URLhttps://www.scopus.com/inward/record.uri?eid=2-s2.0-85086693984&doi=10.1186%2fs12915-020-00795-3&partnerID=40&md5=ad831af3092e549ee40230b57d8ee6f8
DOI10.1186/s12915-020-00795-3
Citation KeyXu2020