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Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation †

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Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation † insects Article β-Cyanoalanine Synthases and Their Possible Role in Pierid Host Plant Adaptation † Anna-Maria Herfurth, Maike van Ohlen ‡ and Ute Wittstock * Institute of Pharmaceutical Biology, Technische Universität Braunschweig, Mendelssohnstrasse 1, D-38106 Braunschweig, Germany; [email protected] (A.-M.-H.); [email protected] (M.O.) * Correspondence: [email protected]; Tel.: +49-531-391-5681 † This manuscript is dedicated to the memory of Professor Thomas Hartmann (Institute of Pharmaceutical Biology, Technische Universität Braunschweig, Braunschweig, Germany). ‡ Present address: SeSaM-Biotech GmbH, Forckenbeckstraße 50, D-52056 Aachen, Germany. Academic Editor: Paul A. Weston Received: 2 May 2017; Accepted: 14 June 2017; Published: 18 June 2017 Abstract: Cyanide is generated in larvae of the glucosinolate-specialist Pieris rapae (Lepidoptera:Pieridae) upon ingestion of plant material containing phenylalanine-derived glucosinolates as chemical defenses. As these glucosinolates were widespread within ancient Brassicales, the ability to detoxify cyanide may therefore have been essential for the host plant shift of Pierid species from Fabales to Brassicales species giving rise to the Pierinae subfamily. Previous research identified β-cyanoalanine and thiocyanate as products of cyanide detoxification in P. rapae larvae as well as three cDNAs encoding the β-cyanoalanine synthases PrBSAS1-PrBSAS3. Here, we analyzed a total of eight species of four lepidopteran families to test if their cyanide detoxification capacity correlates with their feeding specialization. We detected β-cyanoalanine synthase activity in gut protein extracts of all six species tested, which included Pierid species with glucosinolate-containing host plants, Pierids with other hosts, and other Lepidoptera with varying food specialization. Rhodanese activity was only scarcely detectable with the highest levels appearing in the two glucosinolate-feeding Pierids. We then amplified by polymerase chain reaction (PCR) 14 cDNAs encoding β-cyanoalanine synthases from seven species. Enzyme characterization and phylogenetic analysis indicated that lepidopterans are generally equipped with one PrBSAS2 homolog with high affinity for cyanide. A second β-cyanoalanine synthase which grouped with PrBSAS3 was restricted to Pierid species, while a third variant (i.e., homologs of PrBSAS1), was only present in members of the Pierinae subfamily. These results are in agreement with the hypothesis that the host shift to Brassicales was associated with the requirement for a specialized cyanide detoxification machinery. Keywords: glucosinolates; cyanide detoxification; Pieridae; β-cyanoalanine synthase; coevolution 1. Introduction The glucosinolate-myrosinase system serves as an activated chemical defense in plants of the order Brassicales. Upon disruption of the cells, e.g., by herbivores, the glucosinolates, which are amino-acid derived thioglucosides, are hydrolyzed by endogenous thioglucosidases known as myrosinases [1] (Figure1A). This yields products such as isothiocyanates, which are toxic to bacteria, fungi, nematodes and insects (reviewed in [2]). Despite this defense system, glucosinolate-containing plants are colonized by specialist and generalist insects [3–6]. Among the insects that feed exclusively on glucosinolate-containing plants are Pierid species of the Pierinae subfamily like Pieris rapae (Lepidoptera:Pieridae). Larvae of Pieris rapae possess a nitrile specifier protein (NSP) in their gut that redirects glucosinolate breakdown yielding simple nitriles instead of isothiocyanates [7] (Figure1A). NSP activity has also been detected in a range of other glucosinolate-feeding Pierinae and is regarded Insects 2017, 8, 62; doi:10.3390/insects8020062 www.mdpi.com/journal/insects Insects 2017, 8, 62 2 of 17 as the key evolutionary innovation that allowed the host shift of Pierid butterflies to Brassicales about 80 millionInsects years2017, 8, 62 ago [8]. Pierinae which performed a secondary host shift away from Brassicales2 of 16 appear to lack NSP activity [8]. While aliphatic nitriles formed upon glucosinolate metabolism in P. rapaeas the larvaekey evolutionary are excreted, innovation aromatic that allowed nitriles the are host further shift of metabolized Pierid butterfli [es9– to11 Brassicales]. Upon ingestionabout of benzylglucosinolate-containing80 million years ago [8]. Pierinae plant which material, performed the a combinedsecondary host action shift of away plant from myrosinases Brassicales and appear to lack NSP activity [8]. While aliphatic nitriles formed upon glucosinolate metabolism in P. larval NSP results in formation of phenylacetonitrile whose further metabolism is associated with rapae larvae are excreted, aromatic nitriles are further metabolized [9–11]. Upon ingestion of P. rapae the releasebenzylglucosinolate of equimolar-containing amounts plant of material, cyanide the [12 combined] (Figure action1A). of plant myrosinaseslarvae detoxifyand larval cyanideNSP as β-cyanoalanineresults in formation and thiocyanateof phenylacetonitrile indicating whose the further involvement metabolism of isβ associated-cyanoalanine with the synthases release of and rhodanesesequimolar [12] amounts (Figure 1ofB,C). cyanide [12] (Figure 1A). P. rapae larvae detoxify cyanide as β-cyanoalanine and Threethiocyanate gut-expressed indicating theβ-substituted involvement of alanine β-cyanoalanine synthases synthases (BSAS) and withrhodanesesβ-cyanoalanine [12] (Figure 1B, synthaseC). activity, PrBSAS1-PrBSAS3,Three gut-expressed have β-substituted been cloned alanine and characterized synthases (BSAS) from withPieris β rapae-cyanoalanine[13]. In phylogeneticsynthase trees, theyactivity, are embeddedPrBSAS1-PrBSAS3, in bacterial have sequencesbeen cloned together and characterized with uncharacterized from Pieris proteins rapae [13] from. In other lepidopteransphylogenetic and trees with, theyβ-cyanoalanine are embedded synthase in bacterial from sequences the two-spotted together with spider uncharacterized mite, Tetranychus proteins urticae (Trombidiformes:from other lepidoptera Tetranychidae),ns and Tu-CAS with β [-cyanoalanine14]. The mite synthase enzyme hasfrom been the recruitedtwo-spotted by horizontalspider mite, gene Tetranychus urticae (Trombidiformes: Tetranychidae), Tu-CAS [14]. The mite enzyme has been transfer from bacterial endosymbionts [14]. As a likely scenario, the presence of BSAS in lepidopteran recruited by horizontal gene transfer from bacterial endosymbionts [14]. As a likely scenario, the genomespresence is due of toBSAS an in independent lepidopteran genegenomes transfer is due eventto an independent from bacteria gene to transfer ancient event lepidoptera from bacteria [13 ,14]. Thus,to arthropod ancient lepidoptera BSAS are among[13,14]. theThus, few arthropod known examplesBSAS are ofamong horizontal the few gene known transfer examples providing of herbivoreshorizontal with gene tools transfer to overcome providing plant herbivores chemical with defenses tools to [ 15ove].rcome plant chemical defenses [15]. FigureF 1.igureCyanide 1. Cyanide formation formation and and detoxification detoxification in inP. P. rapae rapae.(. (AA)) Formation of of cyanide cyanide upon upon metabolism metabolism of benzylglucosinolateof benzylglucosinolate in P. in rapae P. rapaelarvae. larvae. Aromatic Aromatic glucosinolates glucosinolates are are cleaved cleaved by by plant plant myrosinases myrosinases (Myr).(Myr). In the In the presence presence of of larval larval nitrile nitrile specifier specifier protein protein (NSP), (NSP), phenylacetonitrile phenylacetonitrile is formed is and formed further and furthermetabolized metabolized by by gut gut cytochrome cytochrome P450 P450 enzymes enzymes (CYP) (CYP) yielding yielding instable instable α-hydroxynitrilesα-hydroxynitriles which which decomposedecompose to cyanide to cyanide and aldehydes. and aldehydes. (B) Cyanide (B) Cyanide detoxification detoxification catalyzed catalyzed by β-cyanoalanine by β-cyanoalanine synthase synthase (βCAS). (C) Cyanide detoxification catalyzed by rhodanese (Rho). (βCAS). (C) Cyanide detoxification catalyzed by rhodanese (Rho). Phenylalanine-derived glucosinolates are among the evolutionarily oldest glucosinolates and Phenylalanine-derivedwere widespread in ancient glucosinolates Brassicales [ are16]. amongAs the glucosinolate the evolutionarily-feeding oldestPierinae glucosinolates diverged from and were widespreadmostly Fabales in-feeding ancient Coliadinae Brassicales shortly [16 ].after As the the appearance glucosinolate-feeding of the Brassicales Pierinae [8], larvae diverged of ancient from mostlyPierinae Fabales-feeding were likely Coliadinae confronted shortly mostly after with the this appearance type of glucosinolates of the Brassicales and consequently [8], larvae of with ancient Pierinaecyanide were upon likely glucosinolate confronted mostlymetabol withism. The this ability typeof to glucosinolatescolonize glucosinolate and consequently-containing plants with may cyanide upon glucosinolatetherefore have metabolism.been associated The with ability the ability to colonize to detoxify glucosinolate-containing cyanide [12]. Here, we analyzed plants may a number therefore of Pierid and non-Pierid species with different feeding preferences and evolutionary histories (Figure have been associated with the ability to detoxify cyanide [12]. Here, we analyzed a number of Pierid 2) for β-cyanoalanine synthase and rhodanese activities. We then applied a polymerase chain
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