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Adaptation an Pflanzliche Pyrrolizidinalkaloide Bei Phytophagen Käfern (Coleoptera, Chrysomelidae)

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Adaptation an Pflanzliche Pyrrolizidinalkaloide Bei Phytophagen Käfern (Coleoptera, Chrysomelidae) Adaptation an pflanzliche Pyrrolizidinalkaloide bei phytophagen Käfern (Coleoptera, Chrysomelidae) im Fachbereich Biologie der Universität Hamburg eingereichte Dissertation zur Erlangung des Doktorgrades von Ingo Narberhaus aus Aachen Hamburg 2004 Tag der Disputation: 30.04.2004 Gutachter: Prof. Dr. S. Dobler G Inhalt 1 Einführung 7 2 Uptake and metabolism of pyrrolizidine alkaloids in Longitarsus flea beetles (Coleoptera: Chrysomelidae) adapted and non adapted to alkaloid containing host plants 12 2.1 Summary 12 2.2 Introduction 12 2.3 Material and Methods 14 2.4 Results 18 2.5 Discussion 24 3 Time course of pyrrolizidine alkaloid sequestration in Longitarsus flea beetles (Coleoptera, Chrysomelidae) 27 3.1 Summary 27 3.2 Introduction 27 3.3 Material and Methods 29 3.4 Results 31 3.5 Discussion 35 4 Direct evidence for membrane transport of host plant derived pyrrolizidine alkaloid N-oxides in two leaf beetle genera 38 4.1 Summary 38 4.2 Introduction 38 4.3 Material and Methods 41 4.4 Results 46 4.5 Discussion 54 5 Pyrrolizidine alkaloids on three trophic levels – evidence for toxic and deterrent effects on phytophages and predators 59 5.1 Summary 59 5.2 Introduction 59 5.3 Material and Methods 61 5.4 Results and Discussion 63 6 Abschliessende Diskussion 67 6.1 Speicherung und Metabolisierung von PAs bei Longitarsus 67 6.2 Membran-Carrier für PAs 69 6.3 Strategien der PA-Sequestration im Vergleich 70 6.4 Evolutionäre Aspekte der PA-Adaptation bei Longitarsus 71 6.5 Toxizität von PAs 73 Literatur 76 4 Erklärung Hiermit erkläre ich, dass ich die vorliegende Arbeit selbständig und ohne Benutzung anderer als der angegebenen Hilfsmittel angefertigt habe. Die aus fremden Arbeiten direkt oder indirekt übernommenen Gedanken sind als solche kenntlich gemacht. Die Ergebnisse der Arbeit wurden in den unten aufgeführten vier Beiträgen vorab veröffentlicht bzw. eingereicht; die Hauptkapitel der Dissertation sind in dieser Form, also auch in englischer Sprache, belassen. Teilergebnisse wurden außerdem in Tagungsbei- trägen veröffentlicht. Publikationen NARBERHAUS, I., THEURING, C., HARTMANN, T., DOBLER, S. 2003. Uptake and metabolism of pyrrolizidine alkaloids in Longitarsus flea beetles (Coleoptera: Chrysomelidae) adapted and non adapted to alkaloid containing host plants. Journal of Comparative Physiology 173:483-491. NARBERHAUS, I., THEURING, C., HARTMANN, T., DOBLER, S. 2004. Time course of pyrrolizidine alkaloid sequestration in Longitarsus flea beetles (Coleoptera, Chrysomelidae) Chemoecology 14:17-23. NARBERHAUS, I., PAPKE, U., BEUERLE, T., THEURING, C., HARTMANN, T., DOBLER, S. submitted. Direct evidence for membrane transport of host plant derived pyrrolizidine alkaloid N-oxides in two leaf beetle genera. Journal of Chemical Ecology. NARBERHAUS, I., ZINTGRAF, V., DOBLER, S. submitted. Pyrrolizidine alkaloids on three trophic levels – evidence for toxic and deterrent effects on phytophages and predators. Functional Ecology. Tagungsbeiträge Narberhaus I: Comparative physiology of evolutionary adaptations to host plant alkaloids in a phytophagous beetle genus. 7th Meeting of PhD students in Evolutionary Biology, Bernried 21.3.-24.3.01 (Vortrag) 5 Zintgraf V, I Narberhaus, S Dobler: Zur Evolution des schlechten Geschmacks - Varia- bilität und Funktion der Alkaloid-Sequestration bei Flohkäfern der Gattung Longitarsus (Coleoptera, Chrysomelidae). Graduiertentreffen der Studiengruppe Evolutionsbiologie der DZG, Regensburg, 8.-10.2.02 (Poster) Narberhaus I, S Dobler: Physiologische Anpassungen an Wirtspflanzen-Alkaloide bei Flohkäfern der Gattung Longitarsus. Multitrophische Interaktionen, Göttingen, 11.- 12.4.02 (Vortrag) Narberhaus I, T Hartmann, S Dobler: Physiological adaptations to host plant alkaloids in leaf beetles of the genus Longitarsus. 19th Annual Meeting of the International Society of Chemical Ecology, Hamburg, 3.-8.8.02 (Vortrag) Narberhaus I, T Hartmann, S Dobler: Pyrrolizidine alkaloid sequestration by Longitarsus flea beetles (Coleoptera, Chrysomelidae). DZG-Tagung Berlin, 9.-13.6.03 (Poster) 6 1 Einführung Die Interaktionen zwischen Insekten und Pflanzen sind auf vielfältige Weise von pflanzlichen Inhaltsstoffen abhängig, insbesondere von Sekundärstoffen. Sekundäre Pflanzenstoffe sind Substanzen, die nicht dem pflanzlichen Grundstoffwechsel, sondern eigenen metabolischen Synthesewegen entspringen und dabei keine physiologischen, sondern vorwiegend ökologische Funktionen haben. Sie dienen der Pflanze zum Anlocken von Bestäubern, wirken allelopathisch gegen Konkurrenten, schützen sie als Fungizide oder Bakterizide vor Pathogenen oder als Giftstoffe vor Herbivoren (Harborne, 1995; Schlee, 1992). Etwa ein Drittel der rund 100.000 bekannten pflanzlichen Sekundärstoffe sind Alkaloide. Eine chemisch vielfältige Gruppe darunter, die besondere Relevanz in Tier-Pflanze-Interaktionen hat, sind die Pyrrolizidin-Alkaloide (PAs) (Hartmann, 1991, 1995). Hierbei handelt es sich um Esteralkaloide, bestehend aus einer Necinbase (dem bizyklischen Pyrrolizidin-Kern), die mit einer oder zwei Necinsäuren verestert ist (Abb. 1.1). Sie können als Monoester, offenkettige Diester oder auch als makrocyclische Diester vorkommen. Bisher sind fast 400 verschiedene Strukturen aus ca. 600 Pflanzenarten isoliert und beschrieben worden. PAs sind häufige Inhaltsstoffe in einigen Gattungen der Asteraceae (Tribus Senecioneae und Eupatorieae), in den meisten Boraginaceae und sporadisch in weiteren Pflanzenfamilien (z.B. Fabaceae, Orchidaceae, Apocynaceae) (Hegnauer, 1962-2001; Roeder, 1995). Obgleich es an direkten Belegen mangelt, wird generell davon ausgegangen, dass Pflanzen PAs zur chemischen Verteidigung einsetzen (Boppré, 1990; Hartmann, 1995). Boppré (1986) berichtet von Fütterungstests, in denen Tiere verschiedenster Taxa PA-kontaminierte Nahrung ablehnten, darunter Säuger, Vögel, Reptilien, Amphi- bien und Insekten. Zu proximaten Merkmalen der Tiere wie geschmackliche Erkennung von PAs und Fraßhemmung kann als ultimater Faktor nur die Toxizität der Stoffe führen. Diese ist durch zahlreiche Studien gut belegt. So ist lange bekannt, dass PAs zu ernsthaften Erkrankungen bei Weidetieren oder Menschen führen können (z.B. Fowler, 1968; Kumana et al., 1985; Stillman et al., 1977). PAs wirken bei Wirbeltieren hepatotoxisch und pneumotoxisch (Mattocks, 1986) und, wie durch in vitro Untersuchungen gezeigt wurde, auch neurotoxisch (Schmeller, 1997). Einführung 7 Necinsäure Necinbase Abb. 1.1 Aufbau eines tertiären Pyrrolizidin-Alkaloids (Senecionin). Die salzartigen PA-N-oxide, wie sie in den meisten Pflanzenarten vorkommen, sind jedoch nicht per se toxisch (Hartmann et al., 1989). Erst durch ihre chemische Reduktion werden harmlose N-Oxide zu protoxischen tertiären Alkaloiden („freien Basen“), ein Vorgang, der im reduzierenden Darmmilieu der meisten Herbivoren passiv abläuft. Tertiäre PAs sind lipophil und diffundieren leicht durch biologische Membranen wie die Darmwand. Wenn dies geschieht, können in der Leber eines herbivoren Vertebraten in Folge einer Bioaktivierung durch mikrosomale Cytochrom P-450 Enzyme PAs in instabile Pyrrolverbindungen umgewandelt werden. Dies sind hoch aktive, alkylierende Zwischenprodukte (Winter and Segall, 1989), die mit Proteinen und Nukleinsäuren reagieren und diese damit inaktivieren. Hiermit gehen Veränderungen der Zellfunktionen einher, die bis zum Zelltod oder zur Auslösung einer Karzinogenese führen können (Mattocks, 1986). Einige Säugetierarten besitzen die Möglichkeit einer Re-N-oxidierung von PAs als Entgiftungsmechanismus. Hierbei wird das potentiell toxische tertiäre Alkaloid in sein ungiftiges N-Oxid überführt, welches wiederum nicht in das pyrrolische Toxin umgewandelt werden kann (Cheeke, 1994). Meerschweinchen und Schafe z.B. verfügen über mikrosomale Multisubstrat-Flavin-Monooxygenasen, die eine schnelle Transforma- tion aufgenommener PAs in N-Oxide ermöglichen. Diese N-Oxide werden daraufhin rasch ausgeschieden, was die Resistenz dieser Tiere gegenüber PAs erklärt (Huan et al., 1998a; Huan et al., 1998b; Miranda et al., 1991). Auch bei Insekten werden toxische Effekte von PAs angenommen. Obgleich direkt schädigende Effekte auf Stoffwechsel Einführung 8 und Entwicklung des Individuums bisher sehr mangelhaft überprüft sind, werden hier P- 450-Enzyme mit schädlichen Effekten vermutet, vergleichbar mit denen der Vertebraten (Hodgson, 1985). Nachgewiesen wurde bisher lediglich, u.a. in „wing-spot-tests“ mit Drosophila, eine mutagene Wirkung von PAs (Frei et al., 1992; Zijlstra and Vogel, 1988). Hoch spezialisierte phytophage Insektenarten machen sich die Giftigkeit von PAs bisweilen zunutze. Substanzen, die von der Pflanze als Abwehrstoffe hergestellt werden, werden von diesen eng angepassten Arten nicht nur toleriert, sondern in ihren Körpern aktiv angereichert und dienen ihnen mitunter als Stimulanzien. In einer klassischen Untersuchung am Jakobskrautbär Tyria jacobaeae (Lepidoptera, Arctiidae) zeigten Aplin et al. (1968) zum ersten Mal, dass Insekten PAs in hohen Konzentrationen speichern und teilweise in neue Metaboliten umwandeln können. Später wurde deutlich, dass die Tiere Alkaloide auf diese Weise „recyceln“ und zur Verteidigung gegen ihre eigenen Raubfeinde benutzen (Boppré, 1986; Hartmann, 1999; Hartmann and Witte, 1995; Schneider, 1987). Dieser Vorgang wird als Sequestration bezeichnet. Inzwischen sind PA-sequestrierende Insekten aus diversen Insektentaxa bekannt: aus verschiedenen Gruppen der Lepidoptera, Coleoptera (v.a. Blattkäfern), Orthoptera (der Heuschrecke Zonocerus) und einigen Homoptera
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