Desulfation Followed by Sulfation: Metabolism of Benzylglucosinolate in <i>Athalia rosae</i> (Hymenoptera: Tenthredinidae)

Opitz, Sebastian E. W.; Mix, Andreas; Winde, Inis B.; Müller, Caroline

doi:10.1002/cbic.201100053

Cited by 28 publications

(20 citation statements)

References 38 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…All other known glucosinolate-sequestering herbivores, except for sawfly larvae of the genus Athalia, are sucking insects that may be able to feed without destroying glucosinolate-myrosinase compartmentation (7). In Athalia rosae, glucosinolates are further metabolized to desulfoglucosinolates, glucosinolate-sulfates, and desulfoglucosinolatesulfates before excretion (36), but sulfatase activity comparable to that described in Plutella xylostella (12) could not be detected in A. rosae protein extracts (37). Sulfatase activity assays performed with P. striolata protein extracts also revealed no formation of desulfoglucosinolates (SI Materials and Methods).…”

Section: Discussionmentioning

confidence: 93%

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Beran¹,

Pauchet²,

Kunert

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

112

143

View full text Add to dashboard Cite

The ability of a specialized herbivore to overcome the chemical defense of a particular plant taxon not only makes it accessible as a food source but may also provide metabolites to be exploited for communication or chemical defense. Phyllotreta flea beetles are adapted to crucifer plants (Brassicales) that are defended by the glucosinolate-myrosinase system, the so-called "mustard-oil bomb." Tissue damage caused by insect feeding brings glucosinolates into contact with the plant enzyme myrosinase, which hydrolyzes them to form toxic compounds, such as isothiocyanates. However, we previously observed that Phyllotreta striolata beetles themselves produce volatile glucosinolate hydrolysis products. Here, we show that P. striolata adults selectively accumulate glucosinolates from their food plants to up to 1.75% of their body weight and express their own myrosinase. By combining proteomics and transcriptomics, a gene responsible for myrosinase activity in P. striolata was identified. The major substrates of the heterologously expressed myrosinase were aliphatic glucosinolates, which were hydrolyzed with at least fourfold higher efficiency than aromatic and indolic glucosinolates, and β-O-glucosides. The identified beetle myrosinase belongs to the glycoside hydrolase family 1 and has up to 76% sequence similarity to other β-glucosidases. Phylogenetic analyses suggest species-specific diversification of this gene family in insects and an independent evolution of the beetle myrosinase from other insect β-glucosidases. convergent evolution | host plant specialization P hytophagous insects are confronted with an arsenal of constitutive and inducible chemical plant defenses (1). To avoid deleterious effects from plant toxins, herbivores require appropriate biochemical adaptations allowing them to deal with these metabolites, for example, by developing insensitive target sites or by enzymatic detoxification. Many specialized insects are able to sequester plant defense compounds and exploit them for their own protection against natural enemies and/or as semiochemicals in interspecific communication (2, 3).The glucosinolate-myrosinase system characteristic of plants in the order Brassicales is one of the best-studied activated plant defense systems (4-6), and several different strategies for avoiding glucosinolate toxicity have been described in specialized insect herbivores of the orders Lepidoptera, Hemiptera, and Hymenoptera (7). Glucosinolates are a structurally diverse group of β-thioglucoside-N-hydroxysulfates that are classified according to their precursor amino acid as aliphatic, aromatic, or indolic glucosinolates (6,8). Plant myrosinases, ascorbate-dependent β-thioglucosidases (EC 3.2.1.147) belonging to glycoside hydrolase family 1 (GH1), are stored separately from the glucosinolates and only come into contact with their substrate when the spatial compartmentalization is destroyed, for example, by herbivore feeding (6). The profile of hydrolysis products then depends on glucosinolate structure, cellular conditio...

show abstract

Section: Discussionmentioning

confidence: 93%

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Beran¹,

Pauchet²,

Kunert

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

112

143

View full text Add to dashboard Cite

show abstract

“…The functional basis of adaptation to glucosinolates in the diets of herbivores has been investigated in great detail in several lineages of insect, including the lepidopterans Pieris rapae (Wheat et al 2007) and Plutella xylostella (Ratzka et al 2002), the orthopteran Schistocerca gregaria (Falk and Gershenzon 2007), the sawfly Athalia rosae (Opitz et al 2011), and the aphid Brevicoryne brassicae (Jones et al 2001). In each of these species, single enzymes were identified as essential for detoxification or sequestration of glucosinolate breakdown products that appear to allow for minimal contact with isothiocyanates (Muller et al 2010).…”

Section: Discussionmentioning

confidence: 99%

Genes Involved in the Evolution of Herbivory by a Leaf-Mining, Drosophilid Fly

Whiteman

Gloss

Sackton

et al. 2012

Genome Biology and Evolution

View full text Add to dashboard Cite

Herbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg–adult development time relative to flies reared in glucosinolate knockout (GKO) plants. An analysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. The remaining differentially regulated transcripts also contained a higher proportion of novel genes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.

show abstract

“…Usually, IGs can be subjected to degradation by β-glucosidases in the plant tissue and insect gut producing reactive dialdehydes [47], whereas GSs are degraded by β-thioglucosidases (myrosinases) released in the plants after tissue disruption, which results in the formation of toxic volatile products [48]. The mechanism by which Athalia species avoid this degradation is only partially understood [49].…”

Section: Discussionmentioning

confidence: 99%

Host Shifts from Lamiales to Brassicaceae in the Sawfly Genus Athalia

et al. 2012

Self Cite

View full text Add to dashboard Cite

Plant chemistry can be a key driver of host shifts in herbivores. Several species in the sawfly genus Athalia are important economic pests on Brassicaceae, whereas other Athalia species are specialized on Lamiales. These host plants have glucosides in common, which are sequestered by larvae. To disentangle the possible direction of host shifts in this genus, we examined the sequestration specificity and feeding deterrence of iridoid glucosides (IGs) and glucosinolates (GSs) in larvae of five species which either naturally sequester IGs from their hosts within the Plantaginaceae (Lamiales) or GSs from Brassicaceae, respectively. Furthermore, adults were tested for feeding stimulation by a neo-clerodane diterpenoid which occurs in Lamiales. Larvae of the Plantaginaceae-feeders did not sequester artificially administered p-hydroxybenzylGS and were more deterred by GSs than Brassicaceae-feeders were by IGs. In contrast, larvae of Brassicaceae-feeders were able to sequester artificially administered catalpol (IG), which points to an ancestral association with Lamiales. In line with this finding, adults of all tested species were stimulated by the neo-clerodane diterpenoid. Finally, in a phylogenetic tree inferred from genetic marker sequences of 21 Athalia species, the sister species of all remaining 20 Athalia species also turned out to be a Lamiales-feeder. Fundamental physiological pre-adaptations, such as the establishment of a glucoside transporter, and mechanisms to circumvent activation of glucosides by glucosidases are therefore necessary prerequisites for successful host shifts between Lamiales and Brassicaceae.

show abstract

Desulfation Followed by Sulfation: Metabolism of Benzylglucosinolate in Athalia rosae (Hymenoptera: Tenthredinidae)

Cited by 28 publications

References 38 publications

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Genes Involved in the Evolution of Herbivory by a Leaf-Mining, Drosophilid Fly

Host Shifts from Lamiales to Brassicaceae in the Sawfly Genus Athalia

Contact Info

Product

Resources

About