Transcriptomic analysis of deceptively pollinated Arum maculatum (Araceae) reveals association between terpene synthase expression in floral trap chamber and species-specific pollinator attraction

Abstract

Deceptive pollination often involves volatile organic compound (VOC) emissions that mislead insects into performing non-rewarding pollination. Among deceptively pollinated plants, Arum maculatum is particularly well-known for its potent dung-like VOC emissions and specialized floral chamber, which traps pollinators—mainly Psychoda phalaenoides and P. grisescens—overnight. However, little is known about the genes underlying the production of many A. maculatum VOCs, and their influence on variation in pollinator attraction rates. Therefore, we performed de novo transcriptome sequencing of A. maculatum appendix and male floret tissue collected during- and post-anthesis, from ten natural populations across Europe. These RNA-seq data were paired with GC-MS analyses of floral scent composition and pollinator data collected from the same inflorescences. Differential expression analyses revealed candidate transcripts in appendix tissue linked to malodourous VOCs including indole, p-cresol, and 2-heptanone. Additionally, we found that terpene synthase expression in male floret tissue during anthesis significantly covaried with sex- and species-specific attraction of Psychoda phalaenoides and P. grisescens. Taken together, our results provide the first insights into molecular mechanisms underlying pollinator attraction patterns in A. maculatum, and highlight floral chamber sesquiterpene (e.g. bicyclogermacrene) synthases as interesting candidate genes for further study.

Floral Phytochemistry: Impact of Volatile Organic Compounds and Nectar Secondary Metabolites on Pollinator Behavior and Health

“…In a study on Eucaliptus, susceptibility to L. invasa was associated with γ-terpinene and α-pinene, whereas reduced susceptibility was associated with iso-pinocarveol (29), which may act to recruit parasitoids or have direct toxic effects. [80] Another interesting sesquiterpene, bicyclogermacrene ( 30) is used as part of a deceptive pollination strategy, i. e., as a pheromone mimic which may stimulate the movement of trapped Psychodidae over the male and female florets and is hypothesized to aid in pollination and pollen dispersal, [81] while e,e-αfarnesene (32) is involved in attraction of Andrena pollinators.…”

“…Another interesting sesquiterpene, bicyclogermacrene ( 30 ) is used as part of a deceptive pollination strategy, i. e., as a pheromone mimic which may stimulate the movement of trapped Psychodidae over the male and female florets and is hypothesized to aid in pollination and pollen dispersal, [81] while e,e‐α‐farnesene ( 32 ) is involved in attraction of Andrena pollinators.…”

Characterization of acyl-lipid thioesterase (ALT) enzymes from plants

“…have a strong floral scent profile Szenteczki et al (2022). identified two ALT genes that are upregulated during anthesis in the monocotyledonous flowering plant Arum maculatum, alongside genes encoding distant homologues of the wild tomato ShMKS1 decarboxylase.…”