Dataset Information

Atypical Myrosinase as a Mediator of Glucosinolate Functions in Plants.

ABSTRACT: Glucosinolates (GLSs) are a well-known class of specialized plant metabolites, distributed mostly in the order Brassicales. A vast research field in basic and applied sciences has grown up around GLSs owing to their presence in important agricultural crops and the model plant Arabidopsis thaliana, and their broad range of bioactivities beneficial to human health. The major purpose of GLSs in plants has been considered their function as a chemical defense against predators. GLSs are physically separated from a specialized class of beta-thioglucosidases called myrosinases, at the tissue level or at the single-cell level. They are brought together as a consequence of tissue damage, primarily triggered by herbivores, and their interaction results in the release of toxic volatile chemicals including isothiocyanates. In addition, recent studies have suggested that plants may adopt other strategies independent of tissue disruption for initiating GLS breakdown to cope with certain biotic/abiotic stresses. This hypothesis has been further supported by the discovery of an atypical class of GLS-hydrolyzing enzymes possessing features that are distinct from those of the classical myrosinases. Nevertheless, there is only little information on the physiological importance of atypical myrosinases. In this review, we focus on the broad diversity of the beta-glucosidase subclasses containing known atypical myrosinases in A. thaliana to discuss the hypothesis that numerous members of these subclasses can hydrolyze GLSs to regulate their diverse functions in plants. Also, the increasingly broadening functional repertoires of known atypical/classical myrosinases are described with reference to recent findings. Assessment of independent insights gained from A. thaliana with respect to (1) the phenotype of mutants lacking genes in the GLS metabolic/breakdown pathways, (2) fluctuation in GLS contents/metabolism under specific conditions, and (3) the response of plants to exogenous GLSs or their hydrolytic products, will enable us to reconsider the physiological importance of GLS breakdown in particular situations, which is likely to be regulated by specific beta-glucosidases.

SUBMITTER: Sugiyama R

PROVIDER: S-EPMC6691170 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Atypical Myrosinase as a Mediator of Glucosinolate Functions in Plants.

Sugiyama Ryosuke R Hirai Masami Y MY

Frontiers in plant science 20190806

Glucosinolates (GLSs) are a well-known class of specialized plant metabolites, distributed mostly in the order Brassicales. A vast research field in basic and applied sciences has grown up around GLSs owing to their presence in important agricultural crops and the model plant <i>Arabidopsis thaliana</i>, and their broad range of bioactivities beneficial to human health. The major purpose of GLSs in plants has been considered their function as a chemical defense against predators. GLSs are physic ...[more]

PMID: 31447873

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Project description:BACKGROUND: The glucosinolate-myrosinase system is an activated chemical defense system found in plants of the Brassicales order. Glucosinolates are stored separately from their hydrolytic enzymes, the myrosinases, in plant tissues. Upon tissue damage, e.g. by herbivory, glucosinolates and myrosinases get mixed and glucosinolates are broken down to an array of biologically active compounds of which isothiocyanates are toxic to a wide range of organisms. Specifier proteins occur in some, but not all glucosinolate-containing plants and promote the formation of biologically active non-isothiocyanate products upon myrosinase-catalyzed glucosinolate breakdown. RESULTS: Based on a phytochemical screening among representatives of the Brassicales order, we selected candidate species for identification of specifier protein cDNAs. We identified ten specifier proteins from a range of species of the Brassicaceae and assigned each of them to one of the three specifier protein types (NSP, nitrile-specifier protein, ESP, epithiospecifier protein, TFP, thiocyanate-forming protein) after heterologous expression in Escherichia coli. Together with nine known specifier proteins and three putative specifier proteins found in databases, we subjected the newly identified specifier proteins to phylogenetic analyses. Specifier proteins formed three major clusters, named AtNSP5-cluster, AtNSP1-cluster, and ESP/TFP cluster. Within the ESP/TFP cluster, specifier proteins grouped according to the Brassicaceae lineage they were identified from. Non-synonymous vs. synonymous substitution rate ratios suggested purifying selection to act on specifier protein genes. CONCLUSIONS: Among specifier proteins, NSPs represent the ancestral activity. The data support a monophyletic origin of ESPs from NSPs. The split between NSPs and ESPs/TFPs happened before the radiation of the core Brassicaceae. Future analyses have to show if TFP activity evolved from ESPs at least twice independently in different Brassicaceae lineages as suggested by the phylogeny. The ability to form non-isothiocyanate products by specifier protein activity may provide plants with a selective advantage. The evolution of specifier proteins in the Brassicaceae demonstrates the plasticity of secondary metabolism within an activated plant defense system.

Project description:BACKGROUND:The health of plants is heavily influenced by the intensively researched plant microbiome. The microbiome has to cope with the plant's defensive secondary metabolites to survive and develop, but studies that describe this interaction are rare. In the current study, we describe interactions of endophytic fungi with a widely researched chemical defense system, the glucosinolate - myrosinase - isothiocyanate system. The antifungal isothiocyanates are also of special interest because of their beneficial effects on human consumers. RESULTS:Seven endophytic fungi were isolated from horseradish roots (Armoracia rusticana), from the genera Fusarium, Macrophomina, Setophoma, Paraphoma and Oidiodendron. LC-ESI-MS analysis of the horseradish extract incubated with these fungi showed that six of seven strains could decompose different classes of glucosinolates. Aliphatic, aromatic, thiomethylalkyl and indolic glucosinolates were decomposed by different strains at different rates. SPME-GC-MS measurements showed that two strains released significant amounts of allyl isothiocyanate into the surrounding air, but allyl nitrile was not detected. The LC-ESI-MS analysis of many strains' media showed the presence of allyl isothiocyanate - glutathione conjugate during the decomposition of sinigrin. Four endophytic strains also accepted sinigrin as the sole carbon source. Isothiocyanates inhibited the growth of fungi at various concentrations, phenylethyl isothiocyanate was more potent than allyl isothiocyanate (mean IC50 was 2.30-fold lower). As a control group, ten soil fungi from the same soil were used. They decomposed glucosinolates with lower overall efficiency: six of ten strains had insignificant or weak activities and only three could use sinigrin as a carbon source. The soil fungi also showed lower AITC tolerance in the growth inhibition assay: the median IC50 values were 0.1925 mM for endophytes and 0.0899 mM for soil fungi. CONCLUSIONS:The host's glucosinolates can be used by the tested endophytic fungi as nutrients or to gain competitive advantage over less tolerant species. These activities were much less apparent among the soil fungi. This suggests that the endophytes show adaptation to the host plant's secondary metabolites and that host metabolite specific activities are enriched in the root microbiome. The results present background mechanisms enabling an understanding of how plants shape their microbiome.

Dataset Information

Atypical Myrosinase as a Mediator of Glucosinolate Functions in Plants.

Publications

Atypical Myrosinase as a Mediator of Glucosinolate Functions in Plants.

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