Lineage‐specific evolution of flavin‐containing monooxygenases involved in aliphatic glucosinolate side‐chain modification

• Published in: Journal of systematics and evolution : JSE 2018-03, Vol.56 (2), p.92-104
• Main Authors: Cang, Wei, Sheng, Yu‐Xin, Evivie, Ejiroghene Ruona, Kong, Wen‐Wen, Li, Jing
• Format: Article
• Language: English
• Subjects: Aliphatic compounds; Biological evolution; Brassicaceae; Chains; Chemical synthesis; evolution; Evolutionary genetics; Flavin; flavin‐containing monooxygenases; Gene deletion; Gene expression; Genes; Genomes; Glucosinolates; Metabolites; Methionine; Phylogeny; Progeny; Spatial distribution; Species; Substrates; Synteny; Vegetables
• ISSN: 1674-4918; 1759-6831
• DOI: 10.1111/jse.12289

Glucosinolates, a class of specialized metabolites specific to the order Brassicales, have diverse bioactivities that are largely dependent on the structures of their side chains. Flavin‐containing monooxygenases (FMOs) encoded by the FMOGS‐OX genes have been found to catalyze side‐chain modifications during the synthesis of methionine‐derived aliphatic glucosinolates. Seven FMOGS‐OX genes have been identified in Arabidopsis Heynh., but the evolution of these genes in the Brassicaceae, a family including many economically important vegetables, is poorly understood. In this study, the phylogenetic and syntenic relationships of the FMOGS‐OX genes belonging to 12 sequenced Brassicaceae species were analyzed. Our results showed that the FMOGS‐OX genes included two tandem arrays, the FMOGS‐OX2‐4 group (group A) and the FMOGS‐OX5‐7 group (group B). The evolutionary histories of the FMOGS‐OX groups A and B were similar across the Brassicaceae, but two lineage‐specific evolutionary routes developed after these two separate species lineages diverged from Aethionema arabicum (L.) Andrz. ex DC. In the lineage I route, FMOGS‐OX gene copies tended to increase due to frequent tandem duplication events in most species and a whole genome triplication in Camelina sativa (L.) Crantz. In the lineage II route, gene copies decreased due to deletion events. Combining these results with those of previous studies, we speculated that the FMOGS‐OX genes were derived from an ancestral gene with a broad expression distribution and a broad range of substrates, which then underwent subfunctionalization to generate progeny limited in either spatial expression or substrate structure. Furthermore, the absence of FMOGS‐OX5 substrates in some FMOGS‐OX5‐containing species may suggest neofunctionalization of these genes.