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 (L er ) differed in their hydrolysis products; therefore, the Col ؋ L er 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.

Glucosinolates and other metabolites in the leaves of Arabidopsis thaliana from natural populations and their effects on a generalist and a specialist herbivore

“…Mauricio (1998) found genetic variation for total glucosinolate concentration in four discrete neighboring natural populations of A. thaliana in North Carolina. Glucosinolates accumulation and hydrolysis products are controlled by genetic variation by a number of enzymes that function in a sequential pathway Lambrix et al 2001). Thus a mutation in one of the enzymes or a cross-pollination event could lead to a rapid glucosinolate profile shift from one generation to the next (Kliebenstein 2004).…”

Impact of hydroxylated and non-hydroxylated aliphatic glucosinolates in Arabidopsis thaliana crosses on plant resistance against a generalist and a specialist herbivore

“…On the other hand, less is known about the role of nitriles in plant-insect interactions. Studies with larvae of the generalist Trichoplusia ni (Hübner) revealed a preference for A. thaliana plants producing nitriles as hydrolysis products, whereas isothiocyanates appeared to be rather repellent (Lambrix et al 2001;Zhang et al 2006). In the present study with different A. thaliana GxS lines, classified as isothiocyanate or nitrile producing, derived from the same precursor, either 3MSOP or 3OHP GS, we found no differential effect of the different types of hydrolysis products on larval performance of S. exigua and P. brassicae caterpillars.…”

Glucosinolates: Biosynthesis and Metabolism

“…A QTL affecting the composition of glucosinolate breakdown products has been identified in Arabidopsis (Jander et al, 2001;Lambrix et al, 2001). Based on this QTL, a gene encoding an epithiospecifier protein (ESP) has been cloned (Lambrix et al, 2001).…”

“…Based on this QTL, a gene encoding an epithiospecifier protein (ESP) has been cloned (Lambrix et al, 2001). ESPs have previously been characterized biochemically in different members of the Brassicaceae {Tookey, 1973;MacLeod and Rossiter, 1985).…”