Molecular mechanisms of mutualistic and antagonistic interactions in a plant–pollinator association

Abstract

Many insects metamorphose from antagonistic larvae into mutualistic adult pollinators, with reciprocal adaptation leading to specialized insect-plant associations.It remains unknown how such interactions are established at molecular level. Here we assembled high-quality genomes of a fig species, Ficus pumila var. pumila, and its specific pollinating wasp, Wiebesia pumilae. We combined multi-omics with validation experiments to reveal molecular mechanisms underlying this specialized interaction. In the plant, we identified the specific compound attracting pollinators and validated the function of several key genes regulating its biosynthesis. In the pollinator, we found a highly reduced number of odorant-binding protein (OBP) genes and an OBP mainly binding the attractant. During antagonistic interaction, we found similar chemical profiles and turnovers throughout the development of galled ovules and seeds, and a significant contraction of detoxification-related gene families in the pollinator. Our study detects some key genes bridging coevolved mutualists, establishing expectations for more diffuse insect-pollinator systems.

Adaptation of Fig Wasps (Agaodinae) to Their Host Revealed by Large-Scale Transcriptomic Data

“…Our results demonstrate a dramatic contraction across a wide range of gene families in pollinating fig wasps compared to other Hymenoptera, offering support for results from previous studies [6,33,63,64]. It has been reported that in the genomes of Ceratosolen solmi, Eupristina verticillata, and Wiebesia pumila, many gene families related to chemosensory, detoxification, and innate immune response are reduced [6,33,63,64]. This finding is reflected in our transcriptome study: for the whole family of Agaonidae, the contracted genes families at the level of expression in newly emerged adult fig wasps were mainly enriched in relation to signal transduction and immune response in comparison to other parasitic wasps (Nasonia vitripennis and Copidosoma floridanum), ants, bees, and other Hymenoptera.…”

“…Our results demonstrate a dramatic contraction across a wide range of gene families in pollinating fig wasps compared to other Hymenoptera, offering support for results from previous studies [6,33,63,64]. It has been reported that in the genomes of Ceratosolen solmi, Eupristina verticillata, and Wiebesia pumila, many gene families related to chemosensory, detoxification, and innate immune response are reduced [6,33,63,64].…”

A chromosome-level reference genome of Ensete glaucum gives insight into diversity, chromosomal and repetitive sequence evolution in the Musaceae

“…S1 estimated with k=21 using GenomeScope). Heterozygosity in plants is influenced by mating-systems and pollination [22], life span, habitat fragmentation and cultivation [23]. There is relatively little known about the breeding system and pollination of Ensete species (see [24]) although we observed insects (including the hornet Vespa bicolor, a widespread pollinator in southern China) visiting flowers (Fig.…”

Genome‐wide sequence data show no evidence of hybridization and introgression among pollinator wasps associated with a community of Panamanian strangler figs

“…Bronstein, 1987;Jackson et al, 2008;Kerdelhué et al, 1997;Machado et al, 2005;Molbo et al, 2004;Ramírez, 1970;Sutton et al, 2017;Wang et al, 2016;Wiebes, 1995a). For example, Yang et al (2015) Generally, the blends produced by different figs are sufficiently distinct for wasps to distinguish among potential hosts (Cornille et al, 2012;Grison-Pigé et al, 2002;Hossaert-McKey et al, 2010;Van Noort et al, 1989;Wang, Yang, et al, 2021;Ware et al, 1993). When a female wasp arrives at a fig tree, she must enter a syconium through the ostiole (a small terminal pore) that excludes other insects.…”