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Beetles Do It Differently: Two Stereodivergent Cyclisation Modes in Iridoid-Producing Leaf-Beetle Larvae Maritta Kunert,[A] Peter Rahfeld,[A] Kamel H

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Beetles Do It Differently: Two Stereodivergent Cyclisation Modes in Iridoid-Producing Leaf-Beetle Larvae Maritta Kunert,[A] Peter Rahfeld,[A] Kamel H CHEMBIOCHEM FULL PAPERS DOI: 10.1002/cbic.201200689 Beetles Do It Differently: Two Stereodivergent Cyclisation Modes in Iridoid-Producing Leaf-Beetle Larvae Maritta Kunert,[a] Peter Rahfeld,[a] Kamel H. Shaker,[a] Bernd Schneider,[a] Anja David,[a] Konrad Dettner,[b] Jacques M. Pasteels,[c] and Wilhelm Boland*[a] Larvae of the Chrysomelina species Phaedon cochleariae, Hy- members of the genus Gastrophysa cyclise 8 via a “cisoid dien- drothassa marginella, Phratora vulgatissima, Gastrophysa viridu- amine” intermediate, with exchange of all three deuterium la, Gastrophysa atrocyanea, Gastrophysa cyanea and Gastrophy- atoms from the methyl group at C(3). To study whether the dif- sa polygoni produce the iridoid chrysomelidial (1) to defend ferent cyclisation modes influence the stereochemistry of 1, themselves against predators. Feeding experiments with a deu- the absolute configuration of 1 of the larvae was determined 2 terated precursor ([ H5]8-hydroxygeraniol 9) and in vitro iso- by GC-MS on a chiral column. In accordance with literature (J. 2 tope exchange experiments with defensive secretion in H2O Meinwald, T. H. Jones, J. Am. Chem. Soc. 1978, 100, 1883 and N. revealed differences in the cyclisation of the ultimate precursor Shimizu, R. Yakumaru, T. Sakata, S. Shimano, Y. Kuwahara, J. 8-oxogeranial (8)to1, between members of the genus Gastro- Chem. Ecol. 2012, 38, 29), we found (5S,8S)-chrysomelidial (1) physa and all other species. In P. cochleariae, H. marginella and in H. marginella and P. vulgatissima, but P. cochleariae and all P. vulgatissima 1 is most likely produced by a Rauhut–Currier- investigated members of the genus Gastrophysa synthesise type cyclisation via a “transoid dienamine”, with loss of a (5R,8R)-chrysomelidial (1). single deuterium atom from C(4) of the precursor. In contrast, Introduction Defence mechanisms, such as mechanical, behavioural and chemical responses,[1] have evolved in Chrysomelidae for pro- tection against predation. Chrysomelina larvae respond to dis- turbance and attack by everting dorsal glandular reservoirs to release defensive secretions. Methylcyclopentanoid monoter- penes with an iridane skeleton are widespread constituents of the defensive secretions of phytophagous leaf-beetle larvae of the subtribe Chrysomelina. The principal low-molecular-weight compound of the defensive secretion of the larvae of Phaedon cochleariae, Gastrophysa polygoni, Gastrophysa atrocyanea and Gastrophysa viridula is chrysomelidial (1; Scheme 1, Table 1). Scheme 1. Iridoid defence molecules in insects. In addition to 1, larval secretions of Gastrophysa cyanea con- tain gastrolactone (3), and those of Hydrothassa marginella contain plagiolactone (Table 1). Plagiodial (2) and plagiolactone (4) and iridomyrmecin (5) are components in the blend of the are typical for the larvae of Plagiodera versicolora and Linaeidea Argentine ant Iridomyrmex, which suppress the necrotropho- aenea, and 2 was also found in Prasocuris phellandrii, Phratora retic behaviour of nestmates.[2] Actinidin (6) is produced by Iri- laticollis and Phratora vulgatissima. Larvae of P. vulgatissima domyrmex nitidiceps,[3] and this has a powerful repelling effect show, in addition to 2, a low amount of 1 (Table 1). Dolichodial on their predators. All these compounds share a common bio- synthetic origin, and their biosyntheses proceeds in plants and insects along the same principal pathway, outlined in [a] Dr. M. Kunert, P. Rahfeld, Dr. K. H. Shaker, Dr. B. Schneider, A. David, Scheme 2. Prof. Dr. W. Boland Max Planck Institute for Chemical Ecology In juvenile leaf beetles, the early biosynthetic steps to the iri- [4] Hans-Knoell-Strasse 8, 07745 Jena (Germany) doid monoterpenes take place in the fat body. There, the ter- E-mail: [email protected] penoid backbone of geranyl diphosphate is assembled from [b] Prof. Dr. K. Dettner precursors derived from the mevalonic acid pathway. Hydroxyl- Lehrstuhl Tierçkologie II, Universitt Bayreuth ation and conjugation with glucose generate 8-hydroxygera- Universittsstrasse 30, 95440 Bayreuth (Germany) niol-8-O-b-d-glucoside (7),[4–7] which is transported in the he- [c] Prof. Dr. J. M. Pasteels [8–10] Biologie Evolutive et Ecologie, CP 160/12 Universit Libre de Bruxelles molymph to the glandular reservoir. The final transforma- Avenue Franklin D. Roosevelt 50, 1050 Bruxelles (Belgium) tions involve the hydrolysis of the glucoside and oxidation of 2013 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim ChemBioChem 0000, 00,1–9 &1& These are not the final page numbers! ÞÞ CHEMBIOCHEM FULL PAPERS www.chembiochem.org Chrysomelidial (1) from the essential oil of Actinidia polygama Table 1. Survey of all investigated species and their host plants, and the [13] main low-molecular-weight compounds in insect secretions Miq. served for comparison with the compounds from the larval secretion. The results demonstrate that these leaf-beetle Species Compounds Host plant (family) larvae are able to produce different stereoisomers. P. cochleariae chrysomelidial Brassica rapa subsp. chinensis (Brassicaceae) H. marginella plagiolactone, Ranunculus acris (Ranunculaceae) chrysomelidial Results and Discussion P. vulgatissima plagiodial, Salix caprea (Salicaceae) Feeding and metabolism of [2H ]Ger-8-OH by leaf-beetle chrysomelidial 5 G. viridula chrysomelidial Rumex obtusifolius (Polygonaceae) larvae G. polygoni chrysomelidial Polygonum aviculare (Polygonaceae) G. cyanea chrysomelidial Rumex obtusifolia (Polygonaceae) Insects either synthesise 7 de novo or sequester it from plant [14] [4–7] gastrolactone material as a precursor for the biosynthesis of 1. The glu- G. atrocyanea chrysomelidial Rumex obtusifolia (Polygonaceae) coside is transported in the circulating hemolymph from the P. versicolora plagiodial, Salix fragilis (Salicaceae) fat body to the glandular reservoir, where the final transforma- plagiolactone [8–10] L. aenea plagiodial, Alnus glutinosa (Betulaceae) tions take place. As insects glucosylate the free aglucon to [14] 2 plagiolactone 7, free (2E,6E)-[3-trideuteromethyl,4,4- H5]-3,7-dimethylocta- 2 P. phellandrii plagiodial Caltha palustris (Ranunculaceae) 2,6-diene-1,8-diol ([ H5]Ger-8-OH; 9) could also be used for the P. laticollis plagiodial Populus canadensis (Salicaceae) feeding experiments.[6] Consistent with the previously studied stereochemical course of iridoid biosynthesis,[7,12] loss of a single deuterium atom from C(4) of the precursor was observed in 1 produced by feeding larvae of P. cochleariae (Scheme 3), H. marginella Scheme 2. Principal pathway of the biosynthesis of 1. the two primary hydroxy groups to produce dialdehyde 8.[11,12] Finally, cyclisation of the acyclic dialdehyde 8 generates the iri- doid 1, most likely via a transient plagiodial-type intermediate 2 that is not observed in the secretion. Whether this cyclisation Scheme 3. Metabolism of [ H5]-9 towards 1 in different leaf-beetle larvae. and isomerisation sequence requires two discrete enzymes (Scheme 2) or only a single cyclase (catalysing both steps) re- mains unknown.[6,7] and P. vulgatissima. The same observation was made for 2, [6,7] 2 Lorenz et al. and Veith et al. studied the biosynthesis of generated from [ H5]-9 by the larvae of P. versicolora, P. laticollis, 1 in P. versicolora, G. viridula and P. cochleariae, and used syn- L. aenea, P. vulgatissima and P. phellandrii, as well as for plagio- 2 thetic (2E,6E)-[5,5- H5]2-methylocta-2,6-diene-1,8-diol as a pre- lactone produced by P. versicolora, L. aenea and H. marginella, cursor. They observed loss of a single deuterium atom from and for 3 produced by G. cyanea. The deuterium atoms at the C(4) in nor-chrysomelidial of P. versicolora and P. cochleariae, trideuteromethyl group along with the second deuterium 2 but not in the product of G. viridula. This obvious difference in atom from C(4) of administered [ H5]-9 remained untouched, the mode of cyclisation of the same precursor in two different as evidenced by mass spectroscopy (Figure 1). Under electron leaf-beetle species prompted us to reinvestigate the cyclisation impact conditions, the iridoid skeleton (m/z 166) sequentially of 8-oxogeranial (8) in more detail, by using natural precursors lost the two substituents, thereby leading to a first fragment at labelled with deuterium atoms in mechanistically relevant posi- m/z 138 (ÀCO), and further decomposed with the loss of the · tions. Moreover, the influence of the larval enzymes on the ste- three-carbon unit (ÀC3H5O ) to the cyclopentanoid core frag- reochemistry and configuration of the resulting 1 was studied ment at m/z 81. As evidenced by the shifts from m/z 81 to 85, by gas chromatography on chiral stationary phases. (5R,8S,)- from m/z 109 to 113 and from m/z 138 to 142, the four remain- 2013 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim ChemBioChem 0000, 00,1–9 &2& These are not the final page numbers! ÞÞ CHEMBIOCHEM FULL PAPERS www.chembiochem.org 2 were shaken with H2O without previous addition of unlabelled 9. Interestingly, 1 produced by shaking secretions of all Gastro- 2 physa species in H2O (with and without addition of unlabelled 9) displayed the presence of five deuterium atoms (m/z 171 in- stead of m/z 166). After 10 min, 1% of the peak area belonged to m/z 171; this rose to 4, 7, 9, 27, 61 and 92% after 30, 60, 90, 270 min, 24 h and 4 days, re- spectively (calculated from the intensity of the ion peaks at m/z 166 and 171). The impact of the pH on the isotope exchange was 2 determined after 24 h in H2O, adjusted to pH 5, 6, 8 and 9. At pH 7 we obtained an isotopomer 2 Figure 1. A) Mass fragmentation pattern of unlabelled 1 according to [14]. Mass spectra of B) [ H2]-1 from G. viri- distribution of the molecular 2 2 dula and C) [ H4]-1 from P. cochleariae, feeding for 24 h on leaves treated with [ H5]-9. ion: m/z 167 (2%), 168 (3%), 169 (14%), 170 (18 %), and 171 (63%). Upon changing the pH, ing deuterium atoms were present in these fragments.
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