The defensive function of a pollinator‐attracting floral volatile

Abstract

Benzyl acetone (4‐phenylbutan‐2‐one; BA), the dominant floral fragrance of the wild tobacco Nicotiana attenuata, is known to attract night‐time pollinators, such as Manduca sexta hawkmoths. For this pollinator, BA is not only essential for the pollen transport between conspecific plants, but also for the moth’s short‐distance handling of flowers at night. The emission of BA from the corolla limb, however, starts up to 4 hr before dusk, peaks at dusk and continues throughout the first half of the night. While the function of the nocturnal part of the emission is well studied, the function of the early part of the peak emission remained unknown. By using plants silenced in the expression of the biosynthetic gene of BA (Nachal1), we investigated the function of this early peak emission of BA in the plants´ native habitat in Southwestern Utah. By emitting BA before dusk, N. attenuata is able to prevent the establishment and resulting floral damage by a florivore, the cucumber beetle (Diabrotica undecimpunctata). Plants lacking BA emissions (CHAL) were not only more often colonized by florivores, but also suffered significantly more damage, than control empty vector plants (EV). Choice assays revealed that D. undecimpunctata feeding required the absence of BA. While feeding damage to CHAL flowers was higher than to EV flowers in the early night hours, the effect disappeared during the second half of the night, when flowers stop emitting BA. The close proximity of BA‐emitting flowers to non‐emitting CHAL flowers prevented D. undecimpunctata feeding. In the field, the emission of BA at dusk was sufficient to protect plants for the entire night, as beetles search for new hosts during the early evening hours and remain for the duration of the night, once a host is chosen. Floral BA emission before dusk may have evolved as a consequence of antagonistic interactions with florivores. A single floral volatile can thus simultaneously function as an important floral attractant for pollinators and as effective feeding deterrent against florivores in the same plant species. A plain language summary is available for this article.

Evolution of a novel and adaptive floral scent in wild tobacco

“…Among all co-expressed genes, NaIFR3 , which structurally belongs to the family of NADPH-dependent reductases 17 , showed a similar corolla limb-specific expression to both NaPAL4 and NaCHAL3 (Figure 2B). A kinetic of the transcript abundance showed that NaPAL4 , NaIFR3 and NaCHAL3 are all highly transcribed in the night (Figure 2C), which is consistent to the nocturnal floral emission of BA 6,11 .…”

“…Benzyl acetone (4-phenylbutan-2-one; BA), a dominant nocturnal floral volatile in the wild tobacco species Nicotiana attenuata 6,7 , is known to attract hawkmoth pollinators such as Manduca sexta for outcrossing 8–10 and simultaneously deter feedings from the florivore Diabrotica undecimpunctata 11 . Intriguingly, BA was not found in other Nicotiana species 12 , suggesting that BA is a species-specific floral volatile that underwent rapid evolution.…”

Drought stress alters floral volatiles and reduces floral rewards, pollinator activity, and seed set in a global plant

“…Floral scent serves dual functions in plants, attracting beneficial visitors like pollinators and deterring antagonists such as florivores and nectar robbers (Schiestl et al 2014). In fact, a single floral volatile may act as both an attractant and deterrent, depending on its emission level and the organism receiving the signal (Galen et al 2011, Kessler et al 2019). Pollinators can also learn to associate floral volatiles with reward status and thus use floral volatile blends to select plants (Knauer and Schiestl 2015).…”

Single-cell RNA-sequencing of Nicotiana attenuata petal cells reveals the entire biosynthetic pathway of a floral scent

“…Flowers in the wild tobacco Nicotiana attenuata emit benzylacetone (BA, at night to attract pollinators, such as Manduca sexta hawkmoths (Baldwin, 1997;Haverkamp et al, 2016;Euler and Baldwin, 1996), and to prevent floral damage from cucumber beetles (Kessler et al, 2019). The minor floral scent compounds are benzyl alcohol, cis-3-hexenol, and (E)--bergamotene (Kessler and Baldwin, 2007).…”