Evolution of a Novel and Adaptive Floral Scent in Wild Tobacco.

Many plants emit diverse floral scents that mediate plant-environment interactions and attain reproductive success. However, how plants evolve novel and adaptive biosynthetic pathways for floral volatiles remains unclear. Here, we show that in the wild tobacco, Nicotiana attenuata, a dominant species-specific floral volatile (benzyl acetone, BA) that attracts pollinators and deters florivore is synthesized by phenylalanine ammonia-lyase 4 (NaPAL4), isoflavone reductase 3 (NaIFR3), and chalcone synthase 3 (NaCHAL3). Transient expression of NaFIR3 alone in N. attenuata leaves is sufficient and necessary for ectopic foliar BA emissions, and coexpressing NaIFR3 with NaPAL4 and NaCHAL3 increased the BA emission levels. Independent changes in transcription of NaPAL4 and NaCHAL3 contributed to intraspecific variations of floral BA emission. However, among species, the gain of expression of NaIFR3 resulted in the biosynthesis of BA, which was only found in N. attenuata. This study suggests that novel metabolic pathways associated with adaptation can arise via reconfigurations of gene expression.

Jasmonate signaling makes flowers attractive to pollinators and repellant to florivores in nature.

Flowers are required for the Darwinian fitness of flowering plants, but flowers' advertisements for pollination services can attract florivores. Previous glasshouse work with Nicotiana attenuata revealed the role of jasmonate (JA) signaling in flower development, advertisement and defense. However, whether JA signaling mediates flowers' filtering of floral visitors in nature remained unknown. This field study revealed that silencing JA signaling resulted in flowers that produce less nectar and benzyl acetone, two pollinator-attractive traits. Meanwhile, flowers of defenseless plants were highly attacked by a suite of native herbivores, and damage to buds in native plants correlated negatively with their JA-Ile levels.

Solar flower power.

Bumblebees use invisible temperature patterns on flowers to make foraging decisions.

Tissue-Specific Emission of (E)-α-Bergamotene Helps Resolve the Dilemma When Pollinators Are Also Herbivores.

More than 87% of flowering plant species are animal-pollinated [1] and produce floral scents and other signals to attract pollinators. These floral cues may however also attract antagonistic visitors, including herbivores [2]. The dilemma is exacerbated when adult insects pollinate the same plant that their larvae consume. It remains largely unclear how plants maximize their fitness under these circumstances. Here we show that in the night-flowering wild tobacco Nicotiana attenuata, the emission of a sesquiterpene, (E)-α-bergamotene, in flowers increases adult Manduca sexta moth-mediated pollination success, while the same compound in leaves is known to mediate indirect defense against M. sexta larvae [3, 4]. Forward and reverse genetic analyses demonstrated that both herbivory-induced and floral (E)-α-bergamotene are regulated by the expression of a monoterpene-synthase-derived sesquiterpene synthase (NaTPS38). The expression pattern of NaTPS38 also accounts for variation in (E)-α-bergamotene emission among natural accessions. These results highlight that differential expression of a single gene that results in tissue-specific emission of one compound contributes to resolving the dilemma for plants when their pollinators are also herbivores. Furthermore, this study provides genetic evidence that pollinators and herbivores interactively shape the evolution of floral signals and plant defense.

Innate olfactory preferences for flowers matching proboscis length ensure optimal energy gain in a hawkmoth.

Cost efficient foraging is of especial importance for animals like hawkmoths or hummingbirds that are feeding 'on the wing', making their foraging energetically demanding. The economic decisions made by these animals have a strong influence on the plants they pollinate and floral volatiles are often guiding these decisions. Here we show that the hawkmoth Manduca sexta exhibits an innate preference for volatiles of those Nicotiana flowers, which match the length of the moth's proboscis. This preference becomes apparent already at the initial inflight encounter, with the odour plume. Free-flight respiration analyses combined with nectar calorimetry revealed a significant caloric gain per invested flight energy only for preferred-matching-flowers. Our data therefore support Darwin's initial hypothesis on the coevolution of flower length and moth proboscis. We demonstrate that this interaction is mediated by an adaptive and hardwired olfactory preference of the moth for flowers offering the highest net-energy reward.