The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta

Abstract

The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta Abstract In the genus Petunia, distinct pollination syndromes may have evolved in association with bee-visitation (P. integrifolia spp.) or hawk moth-visitation (P. axillaris spp). We investigated the extent of congruence between floral fragrance and olfactory perception of the hawk moth Manduca sexta. Hawk moth pollinated P. axillaris releases high levels of several compounds compared to the bee-pollinated P. integrifolia that releases benzaldehyde almost exclusively. The three dominating compounds in P. axillaris were benzaldehyde, benzyl alcohol and methyl benzoate. In P. axillaris, benzenoids showed a circadian rhythm with an emission peak at night, which was absent from P. integrifolia. These characters were highly conserved among different P. axillaris subspecies and P. axillaris accessions, with some differences in fragrance composition. Electroantennogram (EAG) recordings using flower-blends of different wild Petunia species on female M. sexta antennae showed that P. axillaris odours elicited stronger responses than P. integrifolia odours. EAG responses were highest to the three dominating compounds in the P. axillaris flower odours. Further, EAG responses to odour-samples collected from P. axillaris flowers confirmed that odours collected at night evoked stronger responses from M. sexta than odours collected during the day. These results show that timing of odour emissions by P. axillaris is in tune with nocturnal hawk moth activity and that flower-volatile composition is adapted to the antennal perception of these pollinators.

Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia

“…Of note is the fact that the common study organism for FVBP research, P. hybrida, is a hybrid of Petunia axillaris and Petunia integrifolia. P. axillaris shows robust oscillation of floral scent in continuous light conditions, but P. integrifolia does not (37). This indicates that the light-and tissue-specific clock phenotypes observed in P. hybrida might be caused by mix of features of P. axillaris and P. integrifolia circadian clocks.…”

Floral Scent Contributes to Interaction Specificity in Coevolving Plants and Their Insect Pollinators

“…At the same time, the floral scent evolution must fit into plant life histories in ways that minimize potential metabolic and ecological costs involved in the scent production (e.g., Gershenzon 1994;Raguso 2008;Wright and Schiestl 2009). Therefore, floral scent emission is expected to peak in association with the peak activity periods of their pollinators (Hoballah et al 2005;Matile and Altenburger 1988;Raguso et al 2003). In Lithophragma, which often depend nearly exclusively on the day-flying Greya moths, scent production was markedly higher in the daytime samples than in the nighttime collections.…”

Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus)

“…In work with S. latifolia and the closely related S. dioica, manipulating the emission of one key volatile, phenylacetaldehyde, had significant effects on pollen transfer; when the two species had similar levels of phenylacetaldehyde, interspecific transmission of pollen increased (Waelti et al, 2008). In Petunia axillaris, genetic manipulation of the production of methyl benzoate influenced both floral attraction and visit order by pollinating hawkmoths (Klahre et al, 2011), despite the presence of multiple other compounds in the floral bouquet, including an equal emission amount of benzaldehyde (Hoballah et al, 2005). Methyl benzoate and other oxygenated aromatic volatiles, like phenylacetaldehyde and benzyl alcohol, strongly activate moth antennal receptor neurons and AL projection neurons (Shields and Hildebrand, 2001;Riffell et al, 2013), thus providing a direct link between the composition of the floral bouquet and sensory processing and behavior.…”

“…deceptive orchid Chiloglottis trapeziformis (Peakall, 1990;Schiestl et al, 1999;Ayasse et al, 2000;Schiestl et al, 2003), where the flower releases the scent mimic of the sex pheromone produced by female Neozeleboria cryptoides wasps in order to attract male wasps as pollinators (Schiestl et al, 2003). Scent can also mediate differential attraction of pollinators between two closely related flower species; for example, Petunia axillaris emits a scent profile attractive to crepuscular moths, whereas bee-and hummingbirdpollinated Petunia (P. integrifolia and P. exserta, respectively) exhibit visual and olfactory characteristics that are attractive to their cognate pollinators (Hoballah et al, 2005;Klahre et al, 2011). Floral scent has also been shown to operate synergistically with the visual display of the flower -an excellent example being the combined effects of the visual and odor display of the Ophrys heldreichii orchid in attracting male Tetralonia berlandi bees (Spaethe et al, 2007).…”