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.

The Versatile Roles of Sulfur-Containing Biomolecules in Plant Defense—A Road to Disease Resistance

“…Interestingly, seeds are unable to de novo synthesize GSLs, therefore, GSL transporters and importers are necessary for loading GSLs into seeds during maturation [175]. GSLs are relatively non-reactive compounds, however, during pathogen infection GSLs are rapidly hydrolyzed by myrosinases to produce different physiologically active toxic compounds such as isothiocyanates, thiocyanates, nitriles and epithionitriles [124,176,177]. The production of various end products of GSLs are organ-specifically regulated in A. thaliana, including the production of nitriles in roots, at the expense of isothiocyanates in rosette leaves [178].…”

Effect of Photoperiod on Chinese Kale (Brassica alboglabra) Sprouts Under White or Combined Red and Blue Light

“…Until now, two atypical myrosinase PEN2/BGLU26 and PYK10/BGLU23 were demonstrated to function in the indole GS turnover in intact plants ( Clay et al, 2009 ; Nakano et al, 2017 ). Recently, in the review of Sugiyama and Hirai, BGLU28 and BGLU30 were proposed to be possibly related to the GS breakdown in sulfur deficiency and darkness condition ( Sugiyama and Hirai, 2019 ). Myrosinase activity can be regulated by multiple environmental factors ( Bhat and Vyas, 2019 ).…”

Glucosinolate Content in Dormant and Germinating Arabidopsis thaliana Seeds Is Affected by Non-Functional Alleles of Classical Myrosinase and Nitrile-Specifier Protein Genes

“…Schlaeppi et al, 2008; Bednarek et al, 2009; Clay et al, 2009; Müller et al, 2010; Stotz et al, 2011; Nakazaki et al, 2019). Due to their unusual structure that includes a sulfate group and a thioglucosidic linkage and may comprise an additional sulfur in the variable side chain ( Figure 1 ), glucosinolates have long been proposed to serve as sulfur storage compounds in addition to their roles as chemical defenses (reviewed in Falk et al, 2007; Sugiyama and Hirai, 2019). In several different species, glucosinolate content has been reported to rise with sulfur supply and to decrease under sulfur deficiency (reviewed in Hirai et al, 2004; Falk et al, 2007).…”

“…Most members of the BGLU18–BGLU33 clade have not been characterized with respect to their activity and specificity with diverse glucosinolates as substrates. In addition, biological roles of BGLU18–BGLU33 that might be associated with activity on glucosinolates are largely unexplored with few exceptions including a role of BGLU18 in herbivore defense and a role of BGLU26 in plant innate immunity (Bednarek et al, 2009; Clay et al, 2009; Nakazaki et al, 2019; Sugiyama and Hirai, 2019).…”