Chemical imitation of yeast fermentation by the drosophilid-pollinated deceptive trap-flower Aristolochia baetica (Aristolochiaceae).

Aristolochia baetica Aristolochiaceae Drosophilidae Phoridae acetoin chemical mimicry deceptive pollination electroantennography floral scents stereochemistry

Journal

Phytochemistry
ISSN: 1873-3700
Titre abrégé: Phytochemistry
Pays: England
ID NLM: 0151434

Informations de publication

Date de publication:
16 May 2024
Historique:
received: 06 02 2024
revised: 08 05 2024
accepted: 12 05 2024
medline: 19 5 2024
pubmed: 19 5 2024
entrez: 18 5 2024
Statut: aheadofprint

Résumé

Deceptive flowers, unlike in mutualistic pollination systems, mislead their pollinators by advertising rewards which ultimately are not provided. Although our understanding of deceptive pollination systems increased in recent years, the attractive signals and deceptive strategies in the majority of species remain unknown. This is also true for the genus Aristolochia, famous for its deceptive and fly-pollinated trap flowers. Representatives of this genus were generally assumed to be oviposition-site mimics, imitating vertebrate carrion or mushrooms. However, recent studies found a broader spectrum of strategies, including kleptomyiophily and imitation of invertebrate carrion. A different deceptive strategy is presented here for the western Mediterranean Aristolochia baetica L. We found that this species is mostly pollinated by drosophilid flies (Drosophilidae, mostly Drosophila spp.), which typically feed on fermenting fruit infested by yeasts. The flowers of A. baetica emitted mostly typical yeast volatiles, predominantly the aliphatic compounds acetoin and 2,3-butandiol, and derived acetates, as well as the aromatic compound 2-phenylethanol. Analyses of the absolute configurations of the chiral volatiles revealed weakly (acetoin, 2,3-butanediol) to strongly (mono- and diacetates) biased stereoisomer-ratios. Electrophysiological (GC-EAD) experiments and lab bioassays demonstrated that most of the floral volatiles, although not all stereoisomers of chiral compounds, were physiologically active and attractive in drosophilid pollinators; a synthetic mixture thereof successfully attracted them in field and lab bioassays. We conclude that A. baetica chemically mimics yeast fermentation to deceive its pollinators. This deceptive strategy (scent chemistry, pollinators, trapping function) is also known from more distantly related plants, such as Arum palaestinum Boiss. (Araceae) and Ceropegia spp. (Apocynaceae), suggesting convergent evolution. In contrast to other studies working on floral scents in plants imitating breeding sites, the present study considered the absolute configuration of chiral compounds.

Identifiants

pubmed: 38762152
pii: S0031-9422(24)00179-1
doi: 10.1016/j.phytochem.2024.114142
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

114142

Informations de copyright

Copyright © 2024. Published by Elsevier Ltd.

Déclaration de conflit d'intérêts

Declaration of Competing Interest ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐ The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Auteurs

Thomas Rupp (T)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria.

Birgit Oelschlägel (B)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany.

Regina Berjano (R)

Department of Vegetal Biology and Ecology, University of Sevilla, Avenida Reina Mercedes s/n, 41012 Sevilla, Spain.

Hafez Mahfoud (H)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany.

Daniele Buono (D)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany.

Torsten Wenke (T)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany.

Katharina Rabitsch (K)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria.

Gerhard Bächli (G)

Institut für Evolutionsbiologie und Umweltforschung, Universität Zürich-Irchel, Winterthurerstrasse 190, 8057 Zürich, Switzerland.

Vesna Stanojlovic (V)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria.

Chiara Cabrele (C)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria.

Wujian Xiong (W)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria; Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianxingxi Road 166, 621000 Mianyang, China.

Markus Knaden (M)

Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans Knoell Strasse 8, 07745 Jena, Germany.

Andreas Dahl (A)

DRESDEN-Concept Genome Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Fetscherstraße 105, 01307 Dresden, Germany.

Christoph Neinhuis (C)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany.

Stefan Wanke (S)

Institut für Botanik, Technische Universität Dresden, Zellescher Weg 20b, 01062 Dresden, Germany; Departamento de Botánica, Instituto de Biología, Universidad Nacional Autonoma de Mexico, Apartado Postal 70-367, 04510 Coyoacan, Distrito Federal, Mexico; Institut für Ökologie, Evolution und Diversiät, Goethe-Universität, Max-von-Laue-Straße 13, 60438 Frankfurt am Main, Germany; Abteilung Botanik und molekulare Evolutionsforschung, Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, 60325 Frankfurt am Main, Germany.

Stefan Dötterl (S)

Department of Environment & Biodiversity, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria. Electronic address: Stefan.Doetterl@plus.ac.at.

Classifications MeSH