Spatial patterning of scent in petunia corolla is discriminated by bees and involves the ABCG1 transporter

Abstract

Floral guides are patterned cues that direct the pollinator to the plant reproductive organs. The spatial distribution of showy visual and olfactory traits allows efficient plant-pollinator interactions. Data on the mechanisms underlying floral volatile patterns or their interactions with pollinators are lacking. Here we characterize the spatial emission patterns of volatiles from the corolla of the model plant Petunia 3 hybrida and reveal the ability of honeybees to distinguish these patterns. Along the adaxial epidermis, in correlation with cell density, the petal base adjacent to reproductive organs emitted significantly higher levels of volatiles than the distal petal rim. Volatile emission could also be differentiated between the two epidermal surfaces: emission from the adaxial side was significantly higher than that from the abaxial side. Similar emission patterns were also observed in other petunias, Dianthus caryophyllus (carnation) and Argyranthemum frutescens (Marguerite daisy). Analyses of transcripts involved in volatile production/emission revealed lower levels of the plasma-membrane transporter ABCG1 in the abaxial versus adaxial epidermis. Transient overexpression of ABCG1 enhanced emission from the abaxial epidermis to the level of the adaxial epidermis, suggesting its involvement in spatial emission patterns in the epidermal layers. Proboscis extension response experiments showed that differences in emission levels along the adaxial epidermis, that is, petal base versus rim, detected by GC-MS are also discernible by honeybees.

Eco-Evo-Devo of petal pigmentation patterning

“…Localised synthesis of chemical pigments is only one component of flowering plants’ palette. It is now evident that the elaboration of physical features such as cell shape and texture, scent emission and the distribution of heat and humidity can also be precisely patterned across the petal surface [ 2 , 3 , 7 , 9 , 92 ]. How these elements impact each other, and to what extent the production of these distinct features is regulated by shared or independent processes remain to be investigated.…”

“…Most petals are not uniformly coloured; some patterns are hidden from us and only detected by animals. Pollinating insects can perceive differences in colour, shape, scent and texture, or a combination of these as well as heat, humidity or even electrical charge gradients on the petal surface [1][2][3][4][5][6][7][8][9]. Pattern elements acting in combination can create complex petal surfaces, but to date, most studies have focused on a single pattern element.…”

A whiff of the future: functions of phenylalanine‐derived aroma compounds and advances in their industrial production

“…Indeed, two factors involved in the active emission of aroma compounds have been identified: the MYB PH4 and adenosine triphosphate‐binding cassette subfamily member 1 (ABCG1) (Adebesin et al ., 2017; Cna'ani et al ., 2015). The latter has also been shown to dictate the spatial pattern of emission from floral tissues (Skaliter et al ., 2021). Whereas the exact mechanism by which PH4 affects emission has yet to be identified, the plasma‐membrane‐localized ABCG1 actively exports aroma compounds from the cell (Adebesin et al ., 2017).…”

“…These results demonstrate the negative ramifications of perturbing crucial metabolic pathways (Mayer et al ., 2001). Vanillin is also a component of scent bouquets of flowers (Knudsen et al ., 2006; Oliva et al ., 2015, 2017; Skaliter et al ., 2021). In petunia flowers, production of vanillin and its derivatives was enhanced by introducing an activator of the phenylpropanoid pathway—the Arabidopsis transcription factor PRODUCTION OF ANTHOCYANIN PIGMENT1 (PAP1) (Fig.…”

Petal Cellular Identities

“…Petunia petals are fused, like petals from the vast majority of asterid flowers ( Endress, 2001 ), and are organized in a tube and limbs ( Figure 1A ). In the limbs, cells are conical and smooth, and their density increases toward the center of the flower, which might influence petal color intensity and levels of emission of volatiles ( Skaliter et al, 2021 ). At the most distal part of the tube, cells appear elongated and covered with striations ( Figure 1A , tube 1).…”