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 adaptive 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 the BA emission level is increased by co-expressing NaIFR3 with NaPAL4 and NaCHAL3 . Independent changes in transcription in all three genes contributed to intraspecific variations of floral BA emission. However, among species, the gain-of-expression in NaIFR3 resulted in the biosynthesis of BA that was only found in N. attenuata . This study suggests that novel metabolic pathways associated with adaptation can arise via re-configurations of gene expression.