The Cellular and Subcellular Organization of the Glucosinolate-Myrosinase System against Herbivores and Pathogens

Abstract

Glucosinolates are an important class of secondary metabolites in Brassicales plants with a critical role in chemical defense. Glucosinolates are chemically inactive but can be hydrolyzed by myrosinases to produce a range of chemically active compounds toxic to herbivores and pathogens, thereby constituting the glucosinolate-myrosinase defense system or the mustard oil bomb. During the evolution, Brassicales plants have developed not only complex biosynthetic pathways for production of a large number of glucosinolate structures but also different classes of myrosinases that differ in catalytic mechanisms and substrate specificity. Studies over the past several decades have made important progress in the understanding of the cellular and subcellular organization of the glucosinolate-myrosinase system for rapid and timely detonation of the mustard oil bomb upon tissue damage after herbivore feeding and pathogen infection. Progress has also been made in understanding the mechanisms that herbivores and pathogens have evolved to counter the mustard oil bomb. In this review, we summarize our current understanding of the function and organization of the glucosinolate-myrosinase system in Brassicales plants and discuss both the progresses and future challenges in addressing this complex defense system as an excellent model for analyzing plant chemical defense.

Keywords: ER body; glucosinolates; mustard bomb; myrosin cells; myrosinases; plant chemical defense.

Figure 1

The glucosinolate–myrosinase defense system. Glucosinolates are hydrolyzed by myrosinases upon tissue damage to generate unstable aglycones, which can rearrange to produce chemically active isothiocyanates, thiocyanates, and nitriles.

Figure 2

Two types of the mustard oil bomb. In the dual-cell type of the mustard bomb, glucosinolates are stored in the S cells, whereas classical myrosinases such as TGG1 and TGG2 from Arabidopsis accumulate in the vacuole of myrosin cells. In the single-cell type mustard oil bomb, atypical myrosinases such as PYK10 and glucosinolates accumulate in the ER bodies and vacuole of the same cell. Upon tissue damage, myrosinases obtain access to glucosinolates to detonate the mustard oil bomb by generating chemically active compounds toxic to herbivores and pathogens. ER, endoplasmic reticulum; PM plasma membrane; MVB, multivesicular body.

Figure 3

Development of myrosin cells in Arabidopsis. Myrosin cells are differentiated from ground meristem cells, which are also the mother cells for vascular cells and mesophyll cells. The FAMA and SCRM transcription factors function as master regulators of both myrosin and guard cell differentiation.

Figure 4

A proposed model for the evolutionary origin of the ER bodies. NAIP proteins are critical components for a family of ER-derived vesicles that are present in all plants. NAIP1 became specialized to be specifically associated with ER bodies through interaction with NAI2. ER bodies accumulate atypical myrosinases such as PYK10 and play a critical role in glucosinolate metabolism in defense against herbivores and pathogens.

Figure 5

Mechanisms by pests and pathogens to counter or exploit the glucosinolate–myrosinase system. These mechanisms include inactivation of glucosinolates by glucosinolate sulfatase (GSS) (1) or sequester glucosinolates from the gut to the body (2). Other pests rely on nitrile-specifier proteins to redirect the glucosinolate hydrolysis from isothiocyanates, which are highly toxic, toward nitriles, which are less toxic (3). Bacterial Pseudomonas pathogens also use Sax proteins to reduce isothiocyanate formation (4). Some adapted specialist insects sequester glucosinolates and convert these glucosinolates to toxic products by using their own myrosinase for defense against predators (5).