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

Abstract

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.

A bird’s-eye view: exploration of the flavin-containing monooxygenase (FMO) superfamily in common wheat

“…Group A FMO s contain all the Arabidopsis FMO-GSOX (glucosinolate oxidase) genes. These FMOs have been experimentally validated to participate in glucosinolate (GSL) biosynthesis by catalyzing the S -hydroxylation of methylthioalkyls to methylsulfinylalkyls, where GSLs are a class of specialized sulphur-containing metabolites involved in plant-herbivory defenses (Cang et al, 2018; Hansen et al, 2007; Kong et al, 2016; Li et al, 2011; Schall et al, 2020). GSLs are predominantly found in the mustard seed family (Brassicaceae), although there is evidence that 500 neighbouring eudicot species outside this family may also contain one or more of the 120 documented GSLs (Flamini, 2012).…”

“…Additionally, a subset of FMOs in A. thaliana have been characterized for their activity in the S -oxygenation of sidechains in various glucosinolate (GSL) compounds (Li et al, 2011). GSLs are potent, specialized defense metabolites found exclusively in the order Brassicales known to play a major role against insect herbivory (Cang et al, 2018; Kong et al, 2016). Grouped as “FMO-GSOXs”, these FMOs, which participate in processing metabolites, play a significant defensive role in plants that produce GSLs.…”

Insights into glucosinolate accumulation and metabolic pathways in Isatis indigotica Fort.

“…Among them, MAM3 and CYP79F2 participate in long-chain aliphatic GSL biosynthesis, while AOP3 catalyzes the transition of methylsulfinylalkyl GSLs to hydroxyalkyl GSLs. Furthermore, FMO GS-OX enzymes could also result in the absence of long-chain aliphatic and hydroxyalkyl GSLs [ 59 ].

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A bird’s-eye view: exploration of the flavin-containing monooxygenase superfamily in common wheat

“…Group A FMOs contain all the Arabidopsis FMO-GSOX (glucosinolate oxidase) genes. These FMOs have been experimentally validated to participate in glucosinolate (GSL) biosynthesis by catalyzing the S-hydroxylation of methylthioalkyls to methylsulfinylalkyls, where GSLs are a class of specialized sulphur-containing metabolites involved in plant-herbivory defenses (Hansen et al, 2007;Li et al, 2011;Kong et al, 2016;Cang et al, 2018;Schall et al, 2020). GSLs are predominantly found in the mustard seed family (Brassicaceae), although there is evidence that 500 neighboring eudicot species outside this family may also contain one or more of the 120 documented GSLs (Flamini, 2012).…”

“…Additionally, a subset of FMOs in A. thaliana have been characterized for their activity in the S-oxygenation of sidechains in various glucosinolate (GSL) compounds (Li et al, 2011). GSLs are potent, specialized defense metabolites found exclusively in the order Brassicales known to play a major role against insect herbivory (Kong et al, 2016;Cang et al, 2018). Grouped as "FMO-GSOXs", these FMOs, which participate in processing metabolites, play a significant defensive role in plants that produce GSLs.…”