The Arabidopsis Epithiospecifier Protein Promotes the Hydrolysis of Glucosinolates to Nitriles and Influences Trichoplusia ni Herbivory

Abstract

Glucosinolates are anionic thioglucosides that have become one of the most frequently studied groups of defensive metabolites in plants. When tissue damage occurs, the thioglucoside linkage is hydrolyzed by enzymes known as myrosinases, resulting in the formation of a variety of products that are active against herbivores and pathogens. In an effort to learn more about the molecular genetic and biochemical regulation of glucosinolate hydrolysis product formation, we analyzed leaf samples of 122 Arabidopsis ecotypes. A distinct polymorphism was observed with all ecotypes producing primarily isothiocyanates or primarily nitriles. The ecotypes Columbia (Col) and Landsberg erecta (Ler) differed in their hydrolysis products; therefore, the Col x Ler recombinant inbred lines were used for mapping the genes controlling this polymorphism. The major quantitative trait locus (QTL) affecting nitrile versus isothiocyanate formation was found very close to a gene encoding a homolog of a Brassica napus epithiospecifier protein (ESP), which causes the formation of epithionitriles instead of isothiocyanates during glucosinolate hydrolysis in the seeds of certain Brassicaceae. The heterologously expressed Arabidopsis ESP was able to convert glucosinolates both to epithionitriles and to simple nitriles in the presence of myrosinase, and thus it was more versatile than previously described ESPs. The role of ESP in plant defense is uncertain, because the generalist herbivore Trichoplusia ni (the cabbage looper) was found to feed more readily on nitrile-producing than on isothiocyanate-producing Arabidopsis. However, isothiocyanates are frequently used as recognition cues by specialist herbivores, and so the formation of nitriles instead of isothiocyanates may allow Arabidopsis to be less apparent to specialists.

Occurrence and formation of indole-3-acetamide in Arabidopsis thaliana

“…iv. The breakdown of glucosinolates predominantly yields nitriles, and only small amounts of isothiocyanates, in the Arabidopsis strain used in our study (Lambrix et al 2001).…”

Functional importance of BAK1 tyrosine phosphorylation in vivo

“…For example, ESP encodes the epithiospecifier protein, which interacts with WRKY53 and promotes the hydrolysis of glucosinolates to nitriles. 42 Accordingly, altered expression of ESP has been shown to influence Trichoplusia ni herbivory. The ESP gene was significantly upregulated (>60 fold) in Y610F plants, suggesting BAK1 is a coreceptor and positive regulator of several signaling pathways, including BR-and flagellin-signaling and is a negative regulator of programmed cell death and, interestingly, phosphorylation of Tyr-610 is required for some but not all functions of BAK1 (Fig.…”

MODIFIED VACUOLE PHENOTYPE1 Is an Arabidopsis Myrosinase-Associated Protein Involved in Endomembrane Protein Trafficking

“…4), only one of which, EPITHIOSPECIFIER MODIFIER1 (ESM1), has been characterized. The gene was identified as part of a quantitative trait locus on chromosome 3 that, in combination with the EPITHIOSPECIFIER PROTEIN (ESP) gene, affected the nitrile-to-isothiocyanate ratio in glucosinolate metabolism (Lambrix et al, 2001;Zhang et al, 2006). The MVP1 expression pattern was examined using the Genevestigator reference expression database and analysis tool (Hruz et al, 2008).…”