Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

Beran, Franziska; Köllner, Tobias G.; Gershenzon, Jonathan; Tholl, Dorothea

doi:10.1111/nph.15718

Cited by 105 publications

(98 citation statements)

References 165 publications

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“…These discoveries raise some fascinating but challenging theoretical questions: First, is this cross-kingdom use of unusual semiochemicals underpinned by convergence at the biosynthetic and molecular levels?S econd, what are the mechanisms that underpin the evolution of pheromone systems comprising combinations of biosynthetically unrelated compounds that are shared among kingdoms?W hile some common secondary metabolites are known to be produced by both plants and insects, examples of the cross-kingdom convergent evolution of semiochemical use are few. [18] Thee xceptions include bark beetles and symbiotic fungi, where both produce bark beetle . Outcomes of sequential two-phase bioassayss howing the response of male Zeleboria thynnine wasps to three different blends of synthetic compounds 1:2:3 in phase 1, with Drakaea micrantha flowers as the control in the dual-choicephase 2.…”

Section: Angewandte Chemiementioning

confidence: 99%

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha

et al. 2019

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Bioactive natural products underpin the intriguing pollination strategy used by sexually deceptive orchids. These compounds, which mimic the sex pheromones of the female insect, are emitted in particular blends to lure male insect pollinators of specific species. By combining methods from field biology, analytical chemistry, electrophysiology, crystallography, and organic synthesis, we report that an undescribed β‐hydroxylactone, in combination with two specific hydroxymethylpyrazines, act as pollinator attractants in the rare hammer orchid Drakaea micrantha. This discovery represents an unusual case of chemically unrelated compounds being used together as a sexual attractant. Furthermore, this is the first example of the identification of pollinator attractants in an endangered orchid, enabling the use of chemistry in orchid conservation. Our synthetic blend is now available to be used in pollinator surveys to locate suitable sites for plant conservation translocations.

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Section: Angewandte Chemiementioning

confidence: 99%

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha

et al. 2019

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“…Upon herbivory, the pro-toxins come into contact with β-glucosidases and are converted to deterrent and toxic compounds (Morant et al, 2008). Such two-component defence systems also evolved in insects and other arthropods, which either sequester or de novo synthesize the glucosylated pro-toxins and produce the corresponding β-glucosidases themselves (Beran, Köllner, Gershenzon, & Tholl, 2019). In contrast to defence strategies that deter the predator before it attacks, two-component defences are usually activated upon injury and thus expose the insect to toxic metabolites.…”

Section: Introductionmentioning

confidence: 99%

Ontogenetic differences in the chemical defence of flea beetles influence their predation risk

2020

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käfern mindestens so hoch ist wie in den Blättern der Futterpflanze, fragten sich die Wissenschaftler, ob sich den Käferlarven damit eine neue Option der Abwehr von Feinden eröffnet, zu denen auch die räuberischen Larven des asiatischen Marienkäfers (Harmonia axyridis, Abbildung 2) gehören. Wurden diesen im Experiment Larven des Meerretticherdflohs angeboten, die Senfölglykoside mit ihrer Nahrung zu sich genommen hatten, hörten die Marienkäferlarven schon nach wenigen Sekunden auf zu fressen, und jede dritte von ihnen erbrach die aufgenommene Mahlzeit. Da die Räuber nach dem Kontakt mit Gift enthaltenden Erdflohkäferlarven schnell lernten, die Artgenossen zu meiden, konnten mehr als zwei Drittel von ihnen überleben. Dagegen wurden Larven, die ernährungsbedingt wenig Senfölglykoside enthielten, von den Marienkäfern bereitwillig gefressen, und 90 Prozent dieser Erdflohkäferlarven überlebten den Angriff nicht. Solche Fütterungsexperimente bestätigten auch die toxische Wirkung der Senfölglykoside auf die Marienkäferlarven. Demnach setzen die Larven der Erdflohkäfer das Gift ihrer Futterpflanze als chemische Waffe für die Abwehr der eigenen Feinde ein. Allerdings wird dadurch nicht jede einzelne Larve geschützt, denn nur wenn einige von ihnen dem Angriff der Räuber zum Opfer fallen, kann die gesamte Population von dem so ausgelösten Lernprozess profitieren. Überraschend war, dass die Marienkäferlarven Eier, Puppen oder ausgewachsene Erdflohkäfer unbeschadet fressen konnten, obwohl diese deutlich mehr Senfölglykoside enthielten als die Erdflohkäferlarven. Und wenn die Räuber die Wahl hatten, bevorzugten sie stets die Puppen vor den Larven. Dieses Paradox erklärten die Wissenschaftler damit, dass vor allem die Larven des Erdflohkäfers in der Lage sind, die Glykoside zu spalten und Senföle freizusetzen, denn sie besitzen etwa 43fach mehr von der dafür benötigten Myrosinase. Deren Aktivität war unabhängig von der aufgenommenen Nahrung und selbst dann nachweisbar, wenn die Larven auf einer Mutante als Futterpflanze gezüchtet wurden, die das pflanzeneigene Enzym nicht bilden konnte. Die Erdflöhe beziehen also nur die Senf-öle von der Futterpflanze. Die zweite Komponente ihrer Abwehrstrategie produzieren die Larven selbst, um die Waffe zu schärfen. Dass dies nur die Larven tun, nicht aber die ausgewachsenen, zum Sprung bereiten Käfer, ist eine bemerkenswerte Anpassung an den durch räuberische Feinde ausgeübten Selektionsdruck. Eine spannende Frage bleibt noch zu lösen: Auch beim Erdflohkäfer werden wie bei den Pflanzen die toxischen Senföle nur nach Verletzungen freigesetzt. Demnach speichert auch der Erdfloh die Senfölglykoside räumlich getrennt von der körpereigenen Myrosinase. Im Experiment lassen sich die beiden Komponenten in Kontakt bringen, indem die Hämolymphe eingefroren und wieder aufgetaut wird, um die darin enthaltenen Zellen zum Platzen zu bringen. Wie der entsprechende Vorgang im Darm des räuberischen Insekts innerhalb kürzester Zeit abläuft, ist bislang noch unklar. Literatur [1] T. Sporer et al., Functional ...

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“…Until recently they had only 108 been described in plants and fungi in the eukaryotic domain, suggesting that insects 109 sequestered terpenes from their diet and were unable to synthesise these compounds de 110 novo (15). In the last decade, insect TPS genes, which are not homologous to plant TPSs, 111 have been discovered in Hemiptera and Coleoptera, and were shown to be involved in the 112 production of aggregation and sex pheromones (1,(22)(23)(24)(25)(26). The enzymes found in Hemiptera 113 are involved in the production of pheromone precursor sesquiterpenes from FPP, although 114 the enzymes catalysing the terminal pheromone biosynthesis steps are unknown (25, 26).…”

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confidence: 99%

“…The TPS of Ips pini also retains IDS 119 function, acting as both a GPPS and TPS in vitro. It is unclear whether the evolution of TPS 120 activity occurred only once in insects, as the most recent phylogenetic evidence suggests, or 121 has occurred independently in different lineages (1, 26).…”

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A novel terpene synthase produces an anti-aphrodisiac pheromone in the butterflyHeliconius melpomene

Darragh

Orteu

Byers

et al. 2019

Preprint

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28Terpenes, a group of structurally diverse compounds, are the biggest class of 29 secondary metabolites. While the biosynthesis of terpenes by enzymes known as terpene 30 synthases (TPSs) has been described in plants and microorganisms, few TPSs have been 31 identified in insects, despite the presence of terpenes in multiple insect species. Indeed, in 32 many insect species, it remains unclear whether terpenes are sequestered from plants or 33 biosynthesised de novo. No homologs of plant TPSs have been found in insect genomes, 34 though insect TPSs with an independent evolutionary origin have been found in Hemiptera 35 and Coleoptera. In the butterfly Heliconius melpomene, the monoterpene (E)-β-ocimene acts 36 as an anti-aphrodisiac pheromone, where it is transferred during mating from males to 37 females to avoid re-mating by deterring males. To date only one insect monoterpene 38 synthase has been described, in Ips pini (Coleoptera), and is a multifunctional TPS and 39 isoprenyl diphosphate synthase (IDS). Here, we combine linkage mapping and expression 40 studies to identify candidate genes involved in the biosynthesis of (E)-β-ocimene. We 41 confirm that H. melpomene has two enzymes that exhibit TPS activity, and one of these, 42HMEL037106g1 is able to synthesise (E)-β-ocimene in vitro. Unlike the enzyme in Ips pini, 43 these enzymes only exhibit residual IDS activity, suggesting they are more specialised TPSs, 44 akin to those found in plants. Phylogenetic analysis shows that these enzymes are unrelated 45 to previously described plant and insect TPSs. The distinct evolutionary origin of TPSs in 46 Lepidoptera suggests that they have evolved multiple times in insects. 47 Significance statement 48 Terpenes are a diverse class of natural compounds, used by both plants and animals 49 for a variety of functions, including chemical communication. In insects it is often unclear 50 whether they are synthesised de novo or sequestered from plants. Some plants and insects 51 have converged to use the same compounds. For instance, (E)-β-ocimene is a common 52 component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-53 aphrodisiac pheromone. We describe two novel terpene synthases, one of which synthesises 54 (E)-β-ocimene in H. melpomene, unrelated not only to plant enzymes but also other recently 55identified insect terpene synthases. This provides the first evidence that the ability to 56 synthesise terpenes has arisen multiple times independently within the insects. 58Plants and insects sometimes use the same compounds for communication (1, 2). 59This may be adaptive if these chemicals exploit pre-existing sensory traits in the intended 60 receiver. For example, sexually deceptive orchids mimic the scent of females of the 61 pollinator species to attract males for pollination (3). Similarly, insects may use plant-like 62 volatiles to exploit the sensory systems of other insects whose sensory systems have evolved 63 for plant-finding (2, 4, 5). Phenotypic convergences s...

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Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites

Cited by 105 publications

References 165 publications

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha

A Specific Blend of Drakolide and Hydroxymethylpyrazines: An Unusual Pollinator Sexual Attractant Used by the Endangered Orchid Drakaea micrantha

Ontogenetic differences in the chemical defence of flea beetles influence their predation risk

A novel terpene synthase produces an anti-aphrodisiac pheromone in the butterflyHeliconius melpomene

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