Abstract
Glucosinolates, a class of secondary metabolites from cruciferous plants, are derived from amino acids and have diverse biological activities, such as in biotic defense, depending on their side chain modification. The first structural modification step in the synthesis of aliphatic (methionine-derived) glucosinolates—S-oxygenation of methylthioalkyl glucosinolates to methylsulfinylalkyl glucosinolates—was found to be catalyzed by five flavin-containing monooxygenases (FMOs), FMOGS-OX1-5. Here, we report two additional FMOGS-OX enzymes, FMOGS-OX6, and FMOGS-OX7, encoded by At1g12130 and At1g12160, respectively. The overexpression of both FMOGS-OX6 and FMOGS-OX7 decreased the ratio of methylthioalkyl glucosinolates to the sum of methylthioalkyl and methylsulfinylalkyl glucosinolates, suggesting that the introduction of the two genes converted methylthioalkyl glucosinolates into methylsulfinylalkyl glucosinolates. Analysis of expression pattern revealed that the spatial expression of the two genes is quite similar and partially overlapped with the other FMOGS-OX genes, which are primarily expressed in vascular tissue. We further analyzed the responsive expression pattern of all the seven FMOGS-OX genes to exogenous treatment with abscisic acid, 1-aminocyclopropane-1-carboxylic acid (ACC), jasmonic acid (JA), salicylic acid, indole-3-acetic acid (IAA), and low and high temperatures. Although these genes showed same tendency toward the changing stimulus, the sensitivity of each gene was quite different. The variety in spatial expression among the FMOGS-OX genes while responding to environmental stimulus indicated a complex and finely tuned regulation of glucosinolates modifications. Identification of these two novel FMOGS-OX enzymes will enhance the understanding of glucosinolates modifications and the importance of evolution of these duplicated genes.
Highlights
Glucosinolates (GSLs) are amino acid-derived natural products primarily present in plants belonging to the Brassicaceae family, such as cabbage, broccoli, and the model plant Arabidopsis thaliana
It was found that At1g12130 and At1g12160 were located in the same subclade, and together with the annotated FMOGS-OX1-5 formed a sevenprotein group (Figure 1A), while At1g12200 was located in a subclade adjacent to the seven-protein group (Figure 1A)
Aliphatic GSLs with side chains of different lengths, including C3, C4, C5, C6, C7, and C8, in the leaf and seed tissues of 35S::FMOGS-OX6, 35S::FMOGS-OX7, and wildtype are shown in Tables 1 and 2
Summary
Glucosinolates (GSLs) are amino acid-derived natural products primarily present in plants belonging to the Brassicaceae family, such as cabbage, broccoli, and the model plant Arabidopsis thaliana. FMOs Involved in Glucosinolates Biosynthesis (Halkier and Gershenzon, 2006; Bones and Rossiter, 2006; Zhang et al, 2006). These breakdown products exert diverse biological effects such as induction of direct toxic effects or other defense responses against pathogens and generalist herbivores (Bednarek et al, 2009; Clay et al, 2009; Hopkins et al, 2009; Laluk et al, 2012). The isothiocyanates derived from some aliphatic (methionine-derived) GSLs are considered to have numerous health benefits including potent anti-cancer property (Fahey et al, 1997, 2002; Rose et al, 2000; Zalcmann and Talalay, 2001). The diverse biological activities of GSLs are largely dependent on the chemical modifications in their side chain
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